Motor Learning

2003 Elsevier Science B.V. All rights reserved Handbook of Neuropsychology, 2nd Edition, Vol. 9 J. Grafman and I.H.
Robertson (Eds)
CHAPTER 5
Motor control and learning principles for rehabilitation of upper limb movements after brain injury
Carolee Winstein a , Alan M. Wing b, and Jill Whitall c
b a Department of Biokinesiology and Physical Therapy, 1540 E. Alcazar Street, CHP-155, Los Angeles, CA 90089-9006, USA Behavioural Brain Sciences Centre, School of Psychology, The University of Birmingham, Edgbaston, Birmingham B15 2TT, UK c Department of Physical Therapy, 100 Penn Street, University of Maryland, Baltimore, MD 21201, USA
Introduction The old adage Practice makes perfect is perhaps most frequently heard in the context of motor skills. Performance improves when people have the opportunity to try out movements and are given feedback about the outcome of those movements so that they can then revise their movements to seek a better outcome. This is as true of normal skills learning as it is of the recovery across a wide range of sensorimotor disabilities (e.g., stroke-hemiparesis, spinal cord-paraplegia, anoxic-cerebral palsy), from central to peripheral (e.g., brain damage to peripheral nerve damage), acute to chronic and young to old. In a 1997 synthesis of intervention trials to improve motor recovery following stroke, Duncan suggested, that the patient will require much more opportunity to practice if motor control is to improve (Duncan, 1997). Indiscriminate practice, however, is not always perfect, rather Perfect practice makes perfect. How can we dene perfect practice? In this chapter we draw on current research in behavioural neuroscience to consider the elements of movement control and what is the relevance to rehabilitation of motor function after brain damage. We take upper limb movement and object manipulation as our
behavioural model and in two core sections cover unimanual action and bimanual skill. In each of these sections we set out three principles of motor control. For each principle we consider the empirical evidence, factors in development and motor learning, the neural bases and the implications for rehabilitation. An important element in our consideration of motor control principles is learning. Indeed, in our opinion, any discussion of rehabilitation for motor control should be informed by a basic understanding of the behavioural and neurobiological mechanisms of human learning and memory. In the nal section of the chapter, we develop and discuss three aspects of motor learning, which apply equally to learning in general, that emerged from the previous sections concerning unimanual and bimanual movements pertinent to the rehabilitation of upper limb movements after brain injury. Before beginning our discussion on principles of motor control for rehabilitation we consider the broader context for research in this area. In particular, we consider the disablement model which treats the relation between pathology, impairment, functional limitation and disability. Impairment, function and disability A general framework for rehabilitation research: the disablement model
Corresponding author. Tel.: +44-121-414-7954 (Reception 4932); Fax: +44-121-414-4897; E-mail: a.m.wing@bham.ac.uk; Web http://www.bham.ac.uk/symon
The use of disablement models as an organising framework for research and practice in physical ther77
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C. Winstein, A.M. Wing and J. Whitall
apy and other rehabilitation professions was one of the key conceptual developments of the 1990s (Jette, 1994). Various models of disablement have been developed and explored, including the World Health Organization (WHO) model, the Nagi model (Nagi, 1965), and the National Center for Medical Rehabilitation Research (NCMRR) model (NIH, 1993). Despite their differences in terminology, each of these models provides a framework for analysis of the impacts of acute and chronic conditions on the functioning of specic body systems, basic human performance, and peoples functioning in necessary, expected, and personally desired roles in society (Jette, 1994). The Nagi disablement model (Nagi, 1965), adopted by the Institute of Medicine in its 1991 report, Disability in America (Pope and Tarlov, 1991), denes four distinct levels in the process of disablement: pathology, impairment, functional limitations, and disability. The Pathology level denes the disease or movement disorder (e.g., multiple sclerosis, cerebral palsy). Impairments are dened at the organ-system level by a loss of structure or function (e.g., paresis, spasticity, limited range of motion); functional limitations are dened at the person-level by a loss of the ability to function in ways considered normal for human beings (e.g., walking, eating, remembering); disabilities are dened at the societal-level by a disadvantage for the person created by the intersection of the impairment or functional limitation with the environment or the persons role in society (e.g., participation in home, work and recreation). A newer version of the WHO model was recently released (December, 2000). This model, referred to as ICIDH-2, has revised terminology with rened denitions for each level (Impairment activityparticipation), but the three basic levels beyond the pathology (i.e., organ, person, and society) still exist (see Fig. 1). The renements in denition are benecial for characterising function where the quality of, or duration of, the activity is lacking. Further, the potential negative connotation associated with disability and handicap in the original model led to the development of new terms, activity and participation, to dene the person and societal level of disability, respectively. Recently, Gordon (2000) proposed the Top-Down model of rehabilitation as the reverse or mirror image of disablement (see
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Fig. 2) that focuses on the enablement process and highlights the process of rehabilitation. With health-care cost containment and a minimal, but growing, body of evidence demonstrating the efcacy of rehabilitation treatment the clinical outcomes research focus has shifted along the disablement continuum (Jette, 1995). Clinical outcomes research in rehabilitation medicine has progressed from earlier work focused exclusively on the impairment level, to more recent work that focuses on the functional limitations or disability level with the development of such scales as the Functional Independence Measure (FIM) which captures the burden of care (i.e., how much assistance is required to accomplish a set of motor and cognitive activities). Jette (1995) supports a paradigm shift in clinical outcomes research from descriptive studies at each level to that which provides direct evidence of the degree to which physical therapy that affects an impairment (e.g., muscle force) will also reduce disability and improve the functional outcomes of the patient (i.e., in activities such as transfers, walking ability, and improved quality of life) (p. 968). In the sections that follow, we focus on the principles of control and learning that are strong candidates for the mediation of functional outcomes through practice protocols in the rehabilitation of upper limb movements after brain injury. Impairments may not directly inuence the disability An implicit but awed assumption regarding the impact of treatment directed at the impairment level is that, if one observes a positive change from a particular intervention at the impairment level (e.g., paresis), this will also increase function and decrease disability. Another questionable assumption is that, if one characterises the recovery pattern of motor control (e.g., Duncan, Goldstein, Matchar et al., 1992), this leads to predictions of disability outcomes. It is now more commonly understood that changes at the impairment level do not directly predict a change in function or disability that is considered clinically meaningful. Indeed, the supposition of weak or nonexistent impairmentfunctiondisability linkages (resulting in lack of recognition of impairment roles in these more distal outcomes) may be seen as equally damaging to effective rehabilitation prac-
Motor control and learning principles for rehabilitation of upper limb movements after brain injury Ch. 5
Health Condition (disorder/disease)
Impairment
Activity
Participation
Contextual a. Environmental b. Personal

Fig. 1. The ICIDH-2 Model of Disablement.
Disablement
Rehabilitation
Disability
Roles
Participation in necessary and desired roles including self -care, social, occupational, and recreational.
Functional Limitations
Skills
Ability to achieve meaningful goals with consistency, flexibility, and efficiency.
Impairments
Resources
Physical and cognitive mechanisms, including musculoskeletal linkages, control of basic movement types, ability to plan, etc.
Pathology
Recovery
Active physiological mechanisms that support recovery and limit future disability.
Fig. 2. Top-Down Model of Rehabilitation (Gordon, 2000).
tice. The need to understand the effectiveness of rehabilitation interventions in the broadest sense includes not only its effect on the individual in terms of impairment (i.e., muscle function) and functional limitation (e.g., reaching and grasping), but also its effect on health-related quality of life and quality of life in general. Relationships between impairments and disabilities are complex and inuenced by many modifying factors (e.g., length of time from disease
onset, physiological capacity, heredity, physical environment, age, psychological and social variables). Thus, the need to understand the fundamental nature of the human movement system both normally and in pathology is perhaps one of the most important goals for research to ultimately impact rehabilitation practice. We suggest that foundational research in movement science can have a useful and long-lasting im79
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pact on rehabilitation practice. The practice of physical rehabilitation evolved in part from practical needs (e.g., WW-II injuries) and was inuenced primarily by a physiologicalmedical perspective. Recently, however, the behavioural, neuropsychological, and neurophysiological science of motor control has had an obvious inuence on the practice of rehabilitation as evidenced by the introduction of such techniques as constraint-induced movement therapy for upper extremity recovery in stroke (Taub and Wolf, 1997) and bodyweight-assisted gait training in spinal cord injury (Harkema, Hurley, Patel et al., 1997) and stroke (Barbeau, McCrea, ODonovan et al., 1999). Both interventions developed out of research using animal models and fundamental questions about how movements are generated, controlled, and coordinated (Hodgson, Roy, de Leon et al., 1994; Nudo, Wise, SiFuentes and Milliken, 1996). Similarly, in a recent research agenda following a 1997 workshop dealing with facilitating patient learning during medical rehabilitation, Fuhrer and Keith (1998), proposed that the effectiveness and efciency of learning-oriented practices will likely be enhanced by well-formulated investigations grounded in available learning theory and research (p. 560). The need to foster translation of the behavioural, biological and physical sciences into clinical practice has been recognised for some time in medicine (Gray and Bonventre, 2002), but only recently recognised specically in rehabilitation. Here, we use the resources section of the Top-Down model to explore the control principles we consider to be the most relevant and promising for the development of rehabilitation of upper limb movement and object manipulation. Current clinical practice: translation from theory? It has been said that it generally takes a decade or so for clinical practice to fully incorporate the ideas and ndings from controlled laboratory research. For example, it normally takes 711 years to complete the developmental steps in the scientic process from discovery to phase-IV clinical trial in determining the effectiveness and long-term effects of any new investigational intervention in rehabilitation (Barbeau and Fung, 2001). For the most part, current clinical practice is not evidence-based for the
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rehabilitation of upper limb movements after brain injury, but instead reects accepted practice and custom, including assumptions that it benets patients (De Weerdt and Feys, 2002; van Vliet and Turton, 2001). Accepted practice and custom are dictated by various approaches (schools of intervention) including the best known neurodevelopmental or Bobath approach (Howle, 2003). Comparative studies between these various schools have not shown that one method is superior to another in the improvement of motor recovery after stroke (Duncan, 1997). These ndings are not particularly surprising when considering that in most cases the hetereogeneity of subjects was high, the interventions were poorly standardised with considerable variability in application across subjects (i.e., patient-tailored programs), and the assessmentoutcome measures were either insensitive or not well matched to the treatment objective. In contrast, over the last 10 years there has been an increase in the number of published papers and small-scale randomised controlled trials describing the systematic application of scientically derived therapy components for rehabilitation of the upper extremity, such as EMG-initiated electrical muscle stimulation (Cauraugh et al., 2001), repetitive training of isolated movements (Butesch, Hummelsheim, Denzler and Mauritz, 1995), and forceduse (Van der Lee, Wagenaar, Lankhorst et al., 1999). In most cases, these therapy components have resulted in a reduction in disability at the resource or skill level of the Top-Down Model. These studies, compared to the approach studies, are more hypothesis-driven and grounded in current theoretical developments derived from the behavioural, biological, and movement sciences. In addition, their design incorporates considerations of critical factors such as initial level of impairment, intensity of treatment (doseresponse), and essential therapeutic components (e.g., strength or function). Current clinical practice is still behind in demonstrating judicious and informed evidence-based decisions that embrace these newer developments. Results of several recent surveys of practicing clinicians (physical and occupational therapists) concerning choice of treatment for stroke rehabilitation in Australia, Sweden, and Britain revealed an inadequate understanding or rationale for the basis of chosen treatments to improve
recovery after stroke (Carr, Mungovan, Shepherd et al., 1994; Nilsson and Nordholm, 1992; Sackley and Lincoln, 1996; Walker, Drummond, Gatt and Sackley, 2000). Similarly, and in spite of mounting evidence showing that repetitive and challenged practice of meaningful tasks in a real-world environment is favourable for motor recovery after stroke, most in-patient stroke units provide relatively limited opportunity for such practice. Lincoln, Willis, Philips et al. (1996) observed patients on a stroke unit and found that the proportion of time spent in therapeutic activity was low; only 36 min/day was spent in contact with a physiotherapist or occupational therapist and in all settings observed, the patients spent many hours doing nothing. Similar results have been reported by others (Keith, 1997; Mackay, Ada, Heard and Adams, 1996). Such ndings of the current practice models and environment for rehabilitation are at considerable odds with the growing evidence for the role of use-dependent and learning-dependent plasticity in the promotion of recovery and rehabilitation (Johansson, 2000). Indeed, Johansson (2000) calls for more translational work with close interaction between basic and applied research to enable the design of rehabilitation strategies based on neurobiological principles in the not-too-distant future. In the sections that follow we provide an attempt at this interaction by reviewing behavioural and neurobiological research as we describe principles of motor control that seem, at least to us, to provide applicable guidelines for rehabilitation. We begin with principles related to unilateral motor control and then cover principles of bilateral control. Where there is applied research we also provide evidence for whether these principles appear to work. However, as noted throughout this essay, we would argue that there is a need for much more good clinical research based on well-established principles founded in basic research into motor control and learning. Reach and grasp: principles for one hand action To set the scene for our review of motor control principles applied to motor rehabilitation, imagine a child given the responsibility of making a cup of tea, unsupervised for the rst time. Standing, somewhat self-consciously, at the kitchen work surface she
thinks through the instructions she has been given, then makes a start by taking one of the mugs hanging from hooks under the cupboard and placing it in front of her. She grasps the handle of the cupboard door with her left hand, opens it and, holding it open, uses the right hand to take out the tin of tea bags. Closing the door she uses both hands to pull the lid off the tin, pick out a tea bag, which she then drops into the mug. She steps to one side, opens the fridge with one hand and bends down to take out a carton of milk with the other, letting the door close by itself as she straightens up. She steps back and puts the milk carton beside the cup. Then, from a drawer, she selects a teaspoon and puts it in the cup. In each of these actions she moves her hand uently. She pauses, perhaps to think through what she must do next. But we will pause to think about what she has already achieved by considering some of the problems her nervous system has had to solve. We may note how hand and arm actions are coordinated, in determining three aspects of effective upper limb function. First, wrist, elbow and shoulder joints work together to take the hand through space towards various targets. Second, the positions of the digits are adjusted during reaching to provide a grasp shaped to allow the target object to be encompassed. Third, the forces exerted by the hand are coordinated with those of the arm in order to lift and transport the gripped object. In this section we use these three aspects of upper limb function to elaborate three principles in the control of upper limb movement and consider their bearing on motor impairment and rehabilitation. The rst principle describes how targeted reaching actions are represented by the central nervous system (CNS) in terms of hand kinematics (the path of the hand expressed in terms of changes with time in position and changes in time derivatives of position). This is in contrast to the kinematics and dynamics (forces, sometimes referred to as kinetics) of the joints required to achieve hand kinematics. The second principle is concerned with the coordination of nger movements that shape the hand with arm movements in reaching for objects in the environment and the role of vision in support of such actions. The third principle focusses on handarm coordination in gripping objects to lift and move them. It states that such manipulative actions involve a combination of feed81
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back (reactive) and feedforward (predictive) control of movement. Principle 1: Movements of the upper limb are represented in hand space Given the jointed nature of the upper limb, hand movements might be expected to follow curved paths. Indeed, if you rest your elbow on the table as you raise your arm, your hand will describe a path that forms an arc of a circle centred on the elbow. However, when reaching freely for an object in the environment or moving an object held in the hand, it may be observed that the path along which the hand moves usually approximates a straight line between start and end-points (Fig. 3). This requires simultaneous coordination of changes in angles of wrist, elbow and shoulder joints. Such coordination can be quite complex, taking account of both kinematic factors (changes in joint angle) and dynamic factors (torques at each joint to produce the angular changes, sometimes referred to as kinetic factors). In this section we consider evidence for, and reasons why, hand movements are organised in terms of straight lines. The fact that movements are produced in straight lines despite kinematic and dynamic complexities leads us to consider possible advantages to organising movements this way. Empirical evidence One of the earliest formal studies drawing attention to the straightness of hand paths was reported by Morasso (1981). Subjects held a handle connected to a 2-link manipulandum, rather like an arm with simple hinges for shoulder and elbow joints that only allowed horizontal movement. The manipulandum recorded x y position of movements that subjects made between a number of positions in the horizontal plane. These positions were marked by lights that came on in sequence to indicate when subjects should move to the next position. The authors reported that the spatial paths were straight lines and the velocity prole had a smooth, single-peaked form regardless of direction. A theoretical account of the form of the velocity prole was subsequently provided by Flash and Hogan (1985). They proposed that the CNS uses a smoothness criterion to organise movement such that the mean squared value of the
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rate of change of acceleration (i.e., the third derivative of position with time or jerk) is minimised. On this assumption they showed that a number of consequences follow including, hand paths should be straight lines and the velocity prole should be Gaussian in form. They also suggested that when a curved path is required by the task (for example in drawing a curved line) this may be achieved by dening minimum jerk trajectory between endpoints that includes a via point at the apex of the curved line. As evidenced by Morassos movement recording apparatus, an arm with two simple hinge joints permits planar x y motion. How much of x y space is covered depends on the lengths of the two segments of the arm. Of course, the human shoulder is not just a simple hinge that opens or closes but allows three directions of rotation (3 degrees of freedom, dfs) exionextension, abduction adduction, internalexternal rotation. So, with the addition of the elbows one df, a total of four available dfs gives two more than the two required for positioning the hand in a plane and one more than needed for positioning in three-dimensional space. Three more dfs are needed for orienting the hand at a particular point in space. For example, in lifting a glass full of water it is important that the angle of the glass relative to the horizontal be preserved to avoid spilling in addition to bringing its position nearer the lips. One of the additional dfs comes from forearm pronationsupination and the wrist confers two more dfs. The shoulder can also affect the angle of the hand relative to the horizontal so, again, the arm provides excess dfs over the minimum requisite count of 3. This means that an object held in the hand can be positioned at a particular orientation in space with many different combinations of arm joint angles. The fact that the multiple joints of the arm allow more than one set of joint angles (i.e., different postures of the upper limb) to achieve the same position and orientation of the end-effector, i.e., the hand, is termed kinematic redundancy. Such redundancy is clearly useful if there are constraints on movement, such as those created by an obstacle in the workspace that limits the positions the elbow can take or constrains the hand approach angle. Thus kinematic constraints on intermediate joint angles are a fac-
(a)
(b)
Elbow extensor torque
Interaction torques
Fig. 3. Centre-out task. The participant makes movements from the centre start point to one of the radially arranged targets. Movement trajectories exhibit some variability and are only approximately straight. Muscle torque (e.g. elbow extensor), which overcomes passive elastic and viscous resistance, at one joint will have interactive effects on other joints (e.g. shoulder and wrist).
tor in planning hand orientation. Another factor in constraining the choice of joint angles is the range of hand movements that a particular combination of shoulder, elbow and wrist joint angles permits. For example, a door handle, requiring clockwise rotation, might be grasped with the right palm facing up or down, but the clockwise rotation needed to operate the handle makes the second option the more obvious choice. In an experimental analog of this situation Rosenbaum, Marchak, Barnes et al. (1990) and Rosenbaum, Vaughan, Barnes and Jorgensen (1992) showed that arm posture in taking hold of an object is constrained by subjective end-state comfort that takes account of both the immediate goal of action and the subsequent movement required of the hand. Multiple joints allow the selection of varied approach paths, but in the absence of constraint the path is usually straight. In order to appreciate the issues for CNS control posed by straight-line paths we consider an alternative view, one that implies that the CNS is only concerned with end-posture (dened by a given set of joint angles that positions the hand at the required location and orientation) and is not concerned with producing straight-line hand paths between postures. Holding a given joint position, say the elbow, against external force disturbances can be achieved by co-activating the agonist and antag-
onist muscles acting around the joint, at the elbow, biceps and brachioradialis opposing triceps. Then, any external displacing force, for example pushing the elbow into extension, results in a restoring force as the agonistantagonist muscle pair are taken out of equilibrium. In the example of the elbow, biceps tension increases, triceps decreases. A greater degree of agonistantagonist co-activation results in more rapid restoration of the original equilibrium position when the displacing force is removed. An inuential theory of movement control (Feldman, 1986) suggested that the CNS organises movement around a joint by selecting agonist and antagonist muscle lengths to produce a new equilibrium position corresponding to the desired angle. Movement to the target is then a function of the time-course of the agonistantagonist muscle length changes, the lengthtension relation for each muscle, and the degree of agonistantagonist coactivation. This model, termed the equilibrium point model, was generalised (Flanagan, Ostry and Feldman, 1993a) to multi-joint movement involving, for example in the case of hand position, shoulder and elbow. Then movement of the hand to the target position is determined by the angular changes at each joint. These reect, not only the lengthtension functions for the muscles at each joint, but also biomechanical interaction effects between movement of one joint
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on movement of the other joints. In a multi-joint system such as the arm, motion at any one joint (e.g., the elbow) produces torque on both proximal and distal segments relating to angular velocity and acceleration terms. These torques have effects on the angles of the proximal (shoulder) and distal (wrist) joints and increase with the speed of movement. One consequence is that, without compensation, interaction torques cause velocity and acceleration dependent distortions of hand path (Hollerbach and Flash, 1982). The straightness of hand paths with movements of different speed thus suggest more active control than is inherent in the basic equilibrium point model. In order to follow a specied trajectory, the equilibrium model could be used with continually updated agonistantagonist torques. However, when this approach is taken for planar two-joint movements, the equilibrium trajectory model proves unsatisfactory in that it implies a greater degree of end-effector stiffness than is actually observed (Gomi and Kawato, 1996). An elegant aspect of the equilibrium point model of movement control is that, in being concerned only with target postures, it avoids computational problems associated with determining the torques required to take the hand along a straight-line path. Since the CNS does appear to seek straight-line paths, it is relevant to ask what might be the gains of doing so? One possibility is that a straight-line path makes evaluation of past progress and prediction of future outcome easier. If a movement is initially poorly directed, for example, because of inaccurate information about target location, if the trajectory is disturbed by external events as it progresses, or if the target itself is moved, it may be easier to detect the discrepancy between intention and performance. We return later to such considerations under Principle 2 of the Reach and grasp section relating to reaching to grasp objects. In the next sub-section we consider rules for learning to produce straight-line paths when these are disturbed through altered environmental conditions. Development and learning Given that adults organise hand movements in straight-line paths, it is interesting to ask how does this feature of movement develop with growth and experience in childhood? It is generally accepted
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that reaching demonstrated before around 4 to 5 months of age is not particularly successful (Bushnell, 1985). Nevertheless, this pre-reaching can be scaffolded to produce more success rather earlier if the infant is given appropriate postural support (e.g., Bower, 1974; von Hofsten, 1982). Konczak and Dichgans (1997) and Konczak, Borutta, Topka and Dichgans (1995) documented the development of stereotypy in hand trajectory in 3-D point-to-point movements from age 5 through 36 months and in adults. In the youngest groups the kinematics of reaching have an ataxic appearance with multiple velocity peaks and very variable interjoint coordination (in terms of relative onset times of shoulder exion and elbow extension and peak elbow and shoulder angular velocities). By 12 months the tangential velocity prole becomes smoother (i.e., fewer velocity peaks) and interjoint coordination is more similar to adults. This process is largely complete and the velocity prole is unimodal by 24 months. However, even by 36 months, the hand path is not as straight as in adults implying that further maturation and/or experience are necessary for adult-like straight path reaching. A number of studies have examined adult learning of straight-line hand movements aimed at point targets. A common paradigm involves the subject holding a 2-joint manipulandum similar to that described earlier, starting each trial at a centre home position and then moving some 30 cm to one of eight positions distributed around the circumference of a circle. A light signals the target position on each trial. If this is selected at random the delay in starting to move (reaction time) can be used as an index of movement preparation processes. Measures of performance include accuracy in hitting the target, movement time, and the straightness of path. This centre-out task is useful in testing a wide range of different combinations of elbow and shoulder angular motion patterns and has proved a fertile method for analysing learning processes contributing to the control of movement. For example, Krakauer, Pine, Ghilardi and Ghez (2000) used the paradigm to study the role of direction and extent in planning reaching movements. In their study subjects did not view the arm directly but observed the progress of their movement in a visual display. This allowed the investigators to introduce changes in the relation be-
tween movement and its displayed outcome in order to study how people learned to overcome altered visuomotor relations. They analysed two types of transformation. In one, a gain change caused errors in the extent of movement and required that subjects learn a new scaling factor for the amplitude of movement. In the other, a rotation of the screen axes induced directional errors and required subjects learn new spatial reference axes. Krakauer et al. (2000) found that learning to re-scale amplitude was faster and generalisation (to previously unvisited targets) was better than with learning rotations. These results suggest that separate processes underlie the learning of direction and extent or that the parameters of a similar process are easier to scale in the latter. Direction and extent relate to kinematics of movement. In a separate study Krakauer, Ghilardi and Ghez (1999) suggested that learning of kinematics is dissociated from the learning of dynamics, that is the forces and torques, associated with movement. Subjects made centre-out aiming movements and, in one condition, were exposed to rotations of the relation between movements and displayed outcome. In another condition an eccentric mass was added to the forearm which caused a change in the limb dynamics. Thus, to produce a straight-line hand path, motor commands had to be changed. Krakauer et al. (1999) examined learning in terms of consolidation and interference to determine if learning of kinematics and dynamics were independent. Learning and consolidation of rotated spatial reference frame and altered intersegmental dynamics, did not interfere with each other. To explain the lack of interference, Krakauer et al. (1999) argued that kinematic and dynamics models are constructed by the CNS in parallel based on errors computed in different coordinate frames. They proposed that hand kinematics were learned from errors in extent and direction in an extrinsic coordinate system (relating to hand path), whereas dynamics are learned from proprioceptive errors in an intrinsic coordinate system (relating to joint motions). Krakauer et al. (1999) argued that learning of kinematics and dynamics are supported by different sensory modalities (visual for hand path, proprioceptive for joint motion) and speculated that these might involve separate working-memory systems. However, recently Tong, Wolpert and Flanagan (2002) have shown interference between learning of
kinematics and dynamics when kinematics in the two learning tasks are equated. On these grounds they suggested that the key factor in determining the separateness of memory representation underlying learning of straight movements is whether or not the kinematic variable (position, velocity, acceleration) is the same. Neural basis We address the neural basis for reaching by rst considering neurophysiological recordings of brain activity (including animal single-unit studies and brain-imaging studies) and then reviewing ndings from studies with patients with specic neurological decits. Single-unit studies of reaching have been described in monkeys performing the centreout task by Georgopoulos and colleagues (for review see Georgopoulos, Taira and Lukashin, 1993). They found that a given neuron in motor cortex tended to respond most strongly when the movement was to be made in one of the eight directions out from the centre. Movements in neighbouring directions elicited a less strong response, while movements in the opposite direction tended to suppress the activity of the unit (relative to its background ring rate). Investigation of a large number of individual units (including studies which extended the paradigm to 3-D space (Schwartz, Kettner and Georgopoulos, 1988) revealed that the frequency of ring of a unit is typically related to the cosine of the angle made by the movement and that units preferred direction. The directional preference of individual units is broadly tuned, thus a given cell res for several neighbouring directions of movement. Georgopoulos and colleagues therefore proposed that movement direction is represented as a vector sum (a population vector) across individual preferred direction vectors of the whole set of units. Signicantly, the neuronal population vector predicts the direction of reaching for movements made from a different origin (Kettner, Schwartz and Georgopoulos, 1988). When monkeys made movements that started from a different centre point, but were parallel in direction to the original movements, the population vector was still closely tuned to the movement direction. The signicance of this proposal is that there is constancy of CNS representation of movement despite biomechanical changes caused by changed disposition of
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the individual joints when starting from a new centre point. Ghilardi, Ghez, Dhawan et al. (2000) used positron emission tomography (PET) images of brain activity in healthy normal subjects to examine brain structures activated by performance of the centre-out task paced by an auditory tone. They contrasted three conditions; predictable target sequence, control-display rotations of between 30 and 60 degrees, and learning a new sequence. Comparing these movement conditions with control conditions in which subjects merely observed visual and auditory events associated with the movement tasks, they obtained an underlying pattern of activation of primary motor and sensory areas, cerebellum and basal ganglia. In addition, right parietal cortex was activated by learning rotations, new sequence learning involved dorsolateral prefrontal cortex (DLPFC) and anterior cingulate. Lesions in different CNS motor structures produce characteristic patterns of motor decit. In humans, the most familiar, and also the most common, motor disorder is unilateral slowness and weakness (hemiparesis) or paralysis (hemiplegia) resulting from a cerebrovascular accident (CVA or stroke). The impaired movement reects lesions in contralateral motor cortex or the pyramidal tract projections from contralateral motor cortex to spinal motor pathways. A characteristic pattern of decit (Colebatch and Gandevia, 1989) is that the distal muscles of the hand are affected to a greater degree than the more proximal muscles of the shoulder and elbow. This is interpreted as reecting the presence of ipsilateral pathways from uninvolved motor cortex that are present in greater proportion in the muscles around proximal joints. As a corollary, control of movement ipsilateral to the stroke is also somewhat impaired, insofar as control of the proximal joints depends in part on ipsilateral pathways from involved motor cortex (Winstein and Pohl, 1995). Slowness and weakness are the primary motor decits in stroke hemiparesis. When hemiparetic subjects are asked to make pointing movements there is evidence of impaired coordination of elbow and shoulder resulting in departure from straightline movements (Levin, 1996). Beer, Dewald and Rymer (2000) analysed limb kinematics and dynamics when stroke patients carried out centre-out
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aiming movements with the weight of the arm supported. They found that patients modulated the initial movement of the hand as target direction varied but that initial movement was systematically misdirected compared to non-paretic or control group arm movements. Their analysis indicated that the effect reected a failure to compensate for passive interaction torques which arise during rapid multi-joint movement. The authors suggest this may reect a failure to predict the limb dynamics due to disuse and, interestingly, note that the difference between paretic and non-paretic appears to be an exaggeration of dominantnondominant limb differences in controls (see also Sainburg and Kalakanis, 2000). As a strategic adaptation to difculty with paretic arm movement, hemiparetic stroke subjects employ trunk movement (Cirstea and Levin, 2000). However, the coordination of the trunk movement with upper limb movement follows a similar pattern as healthy controls when they are asked to reach beyond normal limits. That is, movement of the trunk occurs simultaneously with the upper limb suggesting an anticipatory basis (Levin, Michaelsen, Cirstea and Roby Brami, 2002). Clinical observations (Homes, 1939) indicate an important role of the cerebellum in coordinating multi-joint movement. Bastian, Martin, Keating and Thach (1996) compared subjects with cerebellar lesions and controls reaching to a target directly in front of them. Kinematic analysis showed that, for both slow and fast movements, the cerebellar subjects made abnormally curved wrist paths; the curvature was greater in the slowaccurate condition. In the slow condition, cerebellar subjects showed target undershoot and tended to move one joint at a time (decomposition). In fast reaches, the cerebellar subjects showed target overshoot. In this condition, cerebellar subjects moved the joints at abnormal rates relative to one another, but the movements were less decomposed. Inverse dynamics equations, based on a three-segment limb model, were used to estimate the total torque and various component torques acting at each joint. These component torques comprised torque due to gravity, interaction torques induced by movement of adjacent joints, and torque produced by the muscles and passive tissue elements. Analysis of the torques revealed that subjects with cerebellar lesions produced very different torque proles com-
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pared with controls. In slow reaching, the cerebellar group produced abnormal elbow muscle torques that prevented normal extension of the elbow early in the reach. In fast reaching, they produced inappropriate levels of shoulder muscle torque and also produced elbow muscle torques that did not vary appropriately with the interaction torques affecting the elbow. Lack of appropriate muscle torque resulted in excessive contributions of the interaction torque during the fastaccurate reaches. Bastian et al. (1996) therefore argued that failure of dynamics (the inability to produce muscle torques that compensate for the interaction torques) is an important cause of the classic kinematic decits shown by cerebellar subjects during fast reaching. In the slow condition, they suggested that the observed decomposition of movement represented a strategy used by cerebellar subjects in order to simplify movement by reduction of interaction torques and avoid having to control both joints simultaneously. Impaired interjoint coordination is also seen in neurological patients with absence of proprioceptive feedback which may be interpreted as due to failure of predictive compensation for interaction torques. The most pronounced effect by one joint on its neighbours is when angular motion at that joint reverses direction (when angular acceleration terms dominate). Sainburg, Poizner and Ghez (1993) showed abnormal coordination in deafferented patients making hand movements resembling the slicing action used with a bread knife. The straight-line out-and-back hand path was severely affected at those points where shoulder and elbow angular motions reversed in direction. In a subsequent study (Sainburg, Ghilardi, Poizner and Ghez, 1995) they showed that this arose from poor control over interaction torques. Implications for rehabilitation In considering the implications of straight-line paths for movement rehabilitation we rst consider assessment then training. A typical clinical neurological examination includes evaluation of motor function. For example, the clinician is likely to assess the ability to hold the arms out against gravity and then to ask the patient to move individual joints against resistance. Coordination is commonly tested with the nger nose test in which the patient points al-
ternatively to the testers nger and his own nose while the tester moves the target nger around in space. The movement phase out to the target shows the ability to use immediate vision for action while reaching to point to ones own nose is less dependent on vision and more on proprioception. A classic sign of ataxia is a non-straight hand path taken in homing in on the target. A commonly used standardised clinical test in stroke is the Fugl-Meyer motor assessment (FuglMeyer, Jaasko, Leyman et al., 1975). It consists of a series of observations and tests relating to upper and lower limb function. Depending on the level of ability, each item scores from 0 up to 3. For example one item concerning reaching movements scores (1) if the patient is able to move the arm, but scores (2) if he or she is able to move out of the gross synergy pattern. The results for individual questions are combined to yield an overall score indicating degree of impairment for each area. Our discussion of the centre out task suggests that this might be developed for clinical assessment purposes. For example, the patient might be given a sheet of paper with numbered targets arranged around the perimeter of a circle and a starting position marked in the centre of the circle. Holding a pen, possibly with wide barrel and using a palmar grasp, the patient might then be told to draw a line from the centre out to selected numbers and back, with the numbers called out in turn. Coordination problems would then be revealed by departures form straight-line paths. Of course, due allowance would need to be made for problems such as visuospatial neglect, using appropriate placement of the paper. The task might be carried out in paced manner with and without concurrent vision. Under the heading of training we suggest that, given upper limb movements are represented in hand space, the focus of rehabilitative exercises should be on hand paths rather than on individual joints. Thus, we are sympathetic to neurorehabilitation approaches based on synergy (multi-joint) movement patterns. For example, in the proprioceptive neuromuscular facilitation approach to stroke rehabilitation (PNF, Knott and Voss, 1968), the therapist may take the hemiparetic-stroke patients hand and guide it through straight-line paths which involve multijoint synergies. The therapists other hand may then
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be used to provide guidance or support, say, to the elbow and to provide tactile input over relevant muscles. The PNF methods may also include a quick stretch on the agonist muscle(s) prior to the intended move. As coordination and strength return, the therapist gradually increases the resistance to movement. Given the PNF approach to multi-joint strengthening, it is interesting to note that Ellis, Dawson, Beer and Dewald (2002) developed a multi-joint isometric approach to upper limb movement rehabilitation. They reported reduced torque coupling and increased arm strength following isometric multi-degree of freedom strength training in chronic stroke subjects. Practicing straight-path hand movement provides a natural multi-joint context for therapy with potential of transfer beyond the training situation. Such a multijoint approach might be linked into the approach advocated by Wu and colleagues based on functional tasks where task constraints and goals may help drive action (Trombly and Wu, 1999; Wu, Trombly, Lin and Tickle-Degnen, 1998; Wu, Trombly, Lin and Tickle-Degnen, 2000; Wu, Wong, Lin and Chen, 2001). After stroke, the reduction in muscle power coupled with impaired coordination across joints affects postural stabilisation against gravity and can limit progress in retraining reaching. Practice is more effective if the arm can be supported to provide successful outcome in reaching, and this may underlie recent success achieved with power assistance in an approach to therapy that includes support for the effects of gravity and guidance during forward reaching movements. For example, in a recent study Lum, Burgar, Shor et al. (2002) examined the effect of arm exercises in hemiparetic stroke patients with the hand strapped and wrist immobilised in a splint that was supported by a 6-df robot. The robot was capable of moving, or of being moved with varying degrees of resistance, taking the forearm through a range of positions and orientations in 3-D space. Various straight-line, point-to-point reaching paths were used, chosen to take elbow and shoulder through useful ranges of motion. The protocol included 5 min of unimanual passive movements and 20 min of active movements (which were constrained to follow a correct path). The active movements could be either assisted or resisted. With less impaired subjects, circular as well as point to point paths were included.
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The session also included 12 minutes of bimanual exercises (see Principle 1 of Bilateral movements section). Lum et al. (2002) obtained reliably better results on various assessments including the Fugl-Meyer upper limb (Fugl-Meyer et al., 1975) in the group of patients given this form of exercise over 2 months compared to another group given conventional therapy for the same period of time. In this study the nature of the conventional therapy is not clear. Presumably it would have involved a number of therapists, and each would have tailored his or her approach to the individual needs of a variety of different patients. Some of these approaches might have resulted in performance gains other than on the outcome measures but it is reasonable to suppose that the therapists could have reproduced the actions of the robot with similar or even better results (given the human touch!). Perhaps the fundamental point, here, is that a robot-based approach might be better able to provide the patient with more consistent repetition at the required pace of tailored exercises with more consistent feedback. Although therapy emphasising multi-joint movement may be seen as advantageous it is appropriate to consider, additionally, the contribution of movement components in multi-joint action. Thus, Wing and colleagues (Lough, Wing, Fraser and Jenner, 1984; Wing, Lough, Turton et al., 1990) evaluated the role of the elbow in different upper limb movement patterns. Decits in certain contexts might then encourage the additional focus on that movement context, possibly supplemented by concurrent feedback on the state of particular joints. One innovative approach in this regard is the use of audio feedback in the form of multi-tone patterns, or chords, where individual notes in the chord represent different joint states (Ghez, Rikakis, DuBois et al., 2000). The multidimensional nature of auditory processing lends itself naturally to providing information simultaneously about several different concurrently changing aspects of movement and the listener can then selectively attend to aspects of multi-joint motion which may be causing difculty. Interestingly, the potential for auditory input as part of rehabilitation has also been assayed in a situation where the stimulation provided timing cues for repetitive exercise. Stroke patients made repetitive movements with the paretic
arm in time to a metronome. The trajectories of movements made with the metronome were found to be reliably more consistent in space and time with fewer end-point adjustments (Thaut, Kenyon, Hurt et al., 2002). However, whether or not there was any retention of the improvement after cueing was not documented. Movements of the arm generally involve several joints and hand-path control must make allowance for interaction torques as noted earlier. Bastian, Zackowski and Thach (2002) examined whether cerebellar subjects difculty in coordinating multi-joint upper limb movements would be improved by reducing the number of moving joints by external mechanical xation. Control and cerebellar subjects made elbow exion movements to touch a target under two conditions. Both required just elbow movement, but in one condition the shoulder joint was unconstrained and free to move. In the other condition the shoulder joint was mechanically stabilised so it could not move. Elbow and shoulder torques were estimated using inverse dynamics equations. In the shoulder free condition, cerebellar subjects made greater end-point errors (primarily overshoots) than did controls. Cerebellar subjects overshoot errors were largely due to unwanted exion at the shoulder. The excessive shoulder exion resulted from a torque mismatch, where larger shoulder muscle torques were produced at higher rates than appropriate for a given elbow movement. In the shoulderxed condition, end-point errors of cerebellar subjects and controls were comparable. The improved accuracy of cerebellar subjects was accompanied by reduced shoulder exor muscle activity. Most of the correct cerebellar trials in the shoulder-xed condition were movements made using only muscles that ex the elbow. The ndings of Bastian et al. (2002) conrm that reducing the number of joints to be controlled improves cerebellar movement control. However, it would be premature to suggest that it might form the basis of a rehabilitation technique as it is not known whether such improvements have a carry-over effect to subsequent multi-joint coordination. Indeed it seems more likely that, if there is long-term benet, it will be in improving control over movement at the single-joint level. Control over two-joint movements might be improved by being practiced in a manner
where rigid mechanical constraint at one joint is replaced by damping whose stiffness can be gradually reduced, thus requiring the CNS take increasing control over the interaction torques. Principle 2: Arm movements in reaching are coordinated with hand shaping and are mediated by visual pathways Our earlier example of making a cup of tea included several instances of reaching to take hold of various objects in the environment the mug, the cupboard door, the teabag in the tin, and so on. In each case nger movements are required to shape the hand appropriately to the target of the arms reaching movement. An important observation is that such hand shaping is carried out simultaneously with transport of the hand by the arm. That is, movements of the arm are coordinated with hand shaping and, in this section, we elaborate on this principle in the context of reaching to grasp objects in the environment. Various sources of sensory input contribute to reaching movements. Perhaps the most obvious is vision in the identication of the location of the object as a target for the hand to aim for. Vision is also important for determining the size, shape and orientation of the target so that the hand may be turned and opened appropriately to allow a rm grasp. Contact with the target object results in tactile input from the digits which conrms a successful approach. However, before that proprioceptive inputs from the muscles of the arm and body and also from the vestibular system will have provided information about the initial state of the effector apparatus in order to determine the motor commands required to move toward the target while maintaining balance. Thus, reaching to take hold of an object involves a variety of sensory inputs each providing information on a range of different aspects of the environment which will determine the appropriate coordination of hand, arm and body in the reach to grasp manoeuvre. Thus we may say that motor coordination is based on multiple sensory sources of information. Clearly, somatosensory inputs relating to touch involve neural pathways in the brain that are distinct from those involved in vision. Moreover, cortical pathways for processing tactile and proprioceptive inputs are anatomically distinct. To the extent that
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the pathways are separate, differences may be expected in processing information about tactile events (e.g., contact with a target object) and muscle inputs (e.g., signalling position of the hand). Ultimately the pathways converge, allowing an integrated sense of touch. Distinct cortical pathways have also been identied in the case of vision. These are evident in anatomical terms, with separate projections from primary visual areas in occipital cortex to more dorsal or more ventral portions of parietal cortex. In recent years, it has become apparent that these pathways have functional consequences and, in elaborating our second principle about handarm coordination in reaching, we will include discussion of how vision for conscious perception and vision for immediate action are mediated by separate visual pathways. Empirical evidence Studies of the primate visual system (Ungerleider and Mishkin, 1982) have revealed two major sets of projections from primary visual cortex. One (the ventral stream) runs through a series of cortico cortico connections to inferotemporal cortex, the other (the dorsal stream) links through a series of cortical areas culminating in posterior parietal cortex. Ungerleider and Mishkin (1982) proposed functional consequences of the anatomical separation, with the ventral stream playing an important role in visual recognition of objects, and the dorsal stream responsible for identifying the location of objects. This contrast between what and where functions of vision was very inuential. It led to the proposal of two parallel visuomotor channels for the control of reaching (where) and grasping (what) with relative independence between the transport (guiding the limb to the target) and the grasp component (Jeannerod, 1981; Jeannerod and Prablanc, 1983; Jeannerod, 1984). Numerous studies have shown that the distance between the index nger and thumb (hand aperture) is directly related to the size of the object to be grasped (for review see Smeets and Brenner, 1999). This relation is evident at a point of maximum grip aperture, which occurs well before contact is made with the object. The hypothesised transport and grasp channels are parallel in that greater object size, requiring larger hand aperture, leaves approach largely unchanged and this is the case even when
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object size changes unexpectedly during transport. However, there is a sense in which the two channels are dependent. Aperture timing depends on timing of the transport component. Maximum hand opening during reach-to-grasp occurs quite consistently at approximately 70% of the transport duration, which corresponds to the onset of the deceleration phase associated with homing in on the target object. This is the case even when, in reaching to more distant targets, transport velocity is scaled up so that overall movement duration remains relatively constant and there is approximate constant duration for action. To account for this constancy of phase relations Hoff and Arbib (1993) proposed that coordination of transport and grasp is mediated by an active timing process. Another sense in which the channels for transport and grasp are dependent is that factors that affect the accuracy of hand transport also affect hand aperture. For example, Wing, Turton and Fraser (1986) asked participants to reach for objects, either with eyes closed after the start of movement or as fast as possible. Both types of movement were less accurate in showing more variation in lateral position immediately before contact. However, with less accurate transport, hand aperture was wider, affording a greater degree of tolerance for lower positional accuracy. Such compensation might reect feedback adjustment within each trial. Thus, recognition that the path being taken by the hand is diverging from the straight line from start to target (see Principle 1 of the Reach and grasp section), could trigger wider opening of the hand so that the target will be encompassed within the grasp. However, this would suggest that there should be trial-to-trial positive correlation between departures from the straight-line path and hand aperture and a correlational analysis showed that this was not the case. Wing et al. (1986) therefore concluded that the increase in hand aperture represented strategic adaptation to lower transport accuracy rather than adjustment on the basis of concurrent feedback. The concept of strategic setting of grasp according to limitations in the accuracy of transport is supported by another study of reach to grasp in which participants wore liquid crystal glasses so that the experimenter could determine the presence or absence of vision at the onset of reaching (Jakob-
son and Goodale, 1991). Compared to trial blocks in which vision was consistently available on every trial, in blocks where there was a possibility of removal of vision, maximum hand aperture was wider, whether or not vision was actually withdrawn. This again suggests that aperture in reaching is strategically set in advance in relation to factors likely to inuence transport accuracy. A similar conclusion applies to a study in which transport inaccuracy was introduced by the experimenter (Athenes and Wing, 1989). In this study of reaching to pick up a wine glass containing water, the arm or the target was unexpectedly displaced a few centimetres sideways on a proportion of trials. With straight-line movement paths, such perturbations are readily apparent to participants and could, in principle be readily corrected by an adjustment to trajectory (cf. Paulignan, MacKenzie, Marteniuk and Jeannerod, 1990, Paulignan, MacKenzie, Marteniuk and Jeannerod, 1991). However, Athenes and Wing found that, even on trials where there was no perturbation, the possibility of a perturbation resulted in larger hand aperture than in blocks of trials where there were no perturbations. Studies of reaching and grasping thus do not support the concept of completely separate what and where visual streams. However, there is now growing evidence that suggests another mapping between the anatomy of the visual system and behaviour, one which is based on visual pathways mediating conscious perception versus pathways mediating action (Goodale and Milner, 1992; Milner and Goodale, 1993) (Fig. 4). According to this mapping of function onto anatomy, both streams process information about object size, shape, location. However, each stream uses the visual information in different ways. Ventral stream processing is directed toward cognitive representations that embody enduring characteristics of objects and their semantic relations. Dorsal stream processing is concerned with instantaneous object features that mediate goal-directed action. The contrast between visual processing for perception and for action is nicely illustrated in two neuropsychological case studies, one (RV) involving optic ataxia and the other (DF) visual agnosia (Goodale, Meenan, Bulthoff et al., 1994). RVs optic ataxia, which resulted from bilateral lesions in the occipito-parietal region, meant that she had difculty picking up objects although she had no problems
in identifying them. DF had a visual form agnosia following carbon monoxide poisoning with most damage evident in areas 18 and 19 with 17 spared. Although she was unable to recognise the size, shape and orientation of objects, she had no difculty in picking up blocks placed at varying orientations and posting them like a card through the slot. A direct comparison of the two patients decits was made using a set of planar shapes with smooth boundaries and absence of clear symmetry. In one test, pairs of shapes were presented for judgement of same versus different. The other test involved picking up the shapes. DFs performance in shape discrimination was at chance, whereas RV achieved above 80% correct. In picking up shapes DF chose stable grasp points similar to a normal control, but RV used grasp points that afforded less stable grasp because they did not span the centre of mass of the object. These results thus support the idea of a contrast between a dorsal visual stream subserving immediate action and a ventral stream subserving object perception for decision. Studies with normal participants have also investigated possible dissociation between vision for perception and vision for action. For example, Goodale and colleagues (Agliotti, DeSouza and Goodale, 1995; Haffenden and Goodale, 1998) showed that the apparent size of a centre circle is strongly affected by surrounding circles (Ebbinghaus or Titchener illusion), whereas reaching to grasp the centre circle shows that hand shaping is nearly unaffected by the illusion. Subsequent work has raised some questions about the interpretation of differences in normal participants between the sensitivity of perceptual judgment and control of movement to visual manipulation (e.g., Franz, 2001; Franz, Gegenfurtner, Bulthoff and Fahle, 2000; Vishton, Rea, Cutting and Nunez, 1999). However, this does not account for the earlier neuropsychological results and we return later to implications for rehabilitation of two visual streams for perception and action. Development and learning In the above we noted that hand opening in adults exhibits a maximum aperture that is scaled to object size and that onset of hand closure occurs before and so may be said to anticipate contact with the target object. It is interesting to ask whether the adult
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Posterior parietal cortex Pulvinar Superior colliculus Retina Primary visual cortex Lat Geniculate Pars dorsalis
Dorsal stream
Ventral stream
Inferotemporal cortex
Fig. 4. Schematic representation of the dorsal and ventral visual processing streams.
pattern is present in children. A study of reaching in infants aged from 5 to 13 months showed the onset of hand closing occurred in anticipation of, rather than as a reaction to, contact with the target object (von Hofsten and Rnnqvist, 1988). However, up to age 9 months, hand closure does start later and closer to contact with the target than at age 13 months. Moreover, hand aperture is only scaled with target size from age 9 months. One interpretation of the delayed emergence of the adult pattern of hand arm coordination is that it depends on perceiving properties such as shape and size of the target for reaching and this, in turn, depends on previous manipulation experience with the object. Another factor in the emergence of adult pattern of coordination is that, if adult hand opening is timed in relation to hand transport, knowledge of the abilities of the effector system is required to set appropriate timings. It is likely that this also depends on previous experience with moving the arm and opening the hand. These speculations are supported by prism experiments which show 7-month infants relying on available visual feedback throughout their reach to a target. In contrast, 9-month infants show anticipatory ballistic reaching that is corrected later in the trajectory implying that the initial reach was planned (McDonnell and Abraham, 1979). We return to the
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question of how the CNS makes predictions about effector action under the next principle. Neural basis Neurophysiological studies have provided information on various pathways for vision in action. Using single-unit recording, Rizzolatti, Fogassi and Gallese (1997b) and Rizzolatti, Luppino and Matelli (1998) identied two parietalfrontal circuits which appear to have distinct properties related to reaching and grasping. Thus the ventral intraparietal area VIP and premotor F4 contain bimodal neurons, responding to touch and vision, that relate to guidance of arm movements towards a visual target in 3-D space. In the anterior intraparietal (AIP) and premotor F5 cortex there are neurons responding to visual presentation of 3-D objects of varying size and shape and to grasping aimed at these objects. Gallese, Fadiga, Fogassi et al. (1997) suggest one role for area F5 is the selection of the most suitable type of prehension on the basis of contextual information. Parietal area AIP (anterior intra-parietal sulcus) and ventral premotor area F5 (PMv) in monkey may be critical parts of a cortical circuit which transforms visual information on intrinsic properties of objects into hand movements that allow the animal to grasp the objects appropriately (Rizzolatti, Camarda, Fogassi
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et al., 1988; Taira, Mine, Georgopoulos et al., 1990; see Jeannerod, Arbib, Rizzolatti and Sakata, 1995). Frontal area 5 has direct connections with primary motor cortex (MI) and other subcortical centres for movement execution. For example, neurons located in F5 discharge during active hand and/or mouth movements (Di Pellegrino, Fadiga, Fogassi et al., 1992; Gallese, Fadiga, Fogassi and Rizzolatti, 1996; Rizzolatti, Fadiga, Matelli et al., 1996b; Rizzolatti, Fadiga, Fogassi and Gallese, 1997a). Interestingly, discharge in most F5 neurons correlates with actions, rather than with the individual movements that form the actions, so that F5 neurons may be classied in various categories corresponding to the functional action associated with their discharge. The most common are: grasping-with-the-hand neurons, grasping-with-the-hand-and-the-mouth neurons, manipulating neurons, holding neurons, and tearing neurons. Rizzolatti et al. (1988) thus argued that F5 contains a vocabulary of motor schemas (Arbib, 1981) or action representations. Further study of F5 revealed something unexpected. An individual cell in PMv is active whether the monkey performs a task or observes someone else perform the task. Neurons with this property are called mirror neurons (Gallese et al., 1996; Rizzolatti, Fadiga, Gallese and Fogassi, 1996a). The fact that the same cell is active during action or observation suggests that it is involved in the abstract representation of the motor task. Thus, the relationship between the visual recognition of objects (i.e., familiar objects) and the actions that object allows (the object affordances) that underlies reach and grasp actions has recently been linked to the properties of mirror neurons in PMv of primates (Rizzolatti and Arbib, 1998). However, not all F5 neurons respond to action observation. Mirror neurons are active, both when the monkey performs certain actions and when the monkey observes them performed by others. In contrast, canonical neurons in F5 are active when the monkey performs certain actions but not when the monkey observes actions performed by others. Mirror neurons receive input from the PF region of parietal cortex encoding observations of arm and hand movements. This is in contrast with the canonical F5 neurons which receive object-related input from AIP. In summary, the properties of mirror neurons in monkey suggest that F5 neurons are endowed with an
observationexecution matching system: When the primate observes a motor act that resembles one in its movement repertoire, a representative neural code for this action is automatically retrieved (implicit retrieval). This code involves the activation of a subset of cortical units, the mirror neurons of F5, which discharge when the observed act is executed by the monkey itself. Earlier we considered neuropsychological evidence for two visual processing streams. Imaging studies have helped elucidate the dissociation between visual processing routes. For example, James, Humphrey, Gati et al. (2002) carried out an fMRI in a priming study. They found that an area in ventral temporo-occipital cortex, which is part of the human homolog of the ventral stream of visual processing, exhibited priming for both identical and depthrotated images of objects. An area in the caudal part of the intraparietal sulcus also showed priming, but only with identical images of objects. This dorsalstream area treated rotated images as new objects. The authors suggest that difference in the pattern of priming-related activation in the two areas may reect the respective roles of the ventral and dorsal streams in object recognition and object-directed action. Having reviewed neurophysiological studies of brain function underlying reach to grasp actions we now turn to consider neuropsychological studies of the effects of brain damage. We have already described the studies of Goodale and colleagues making the case for a distinction between separate visual processing streams for perception and action. We now ask what do studies of neurological patients with motor disorders tell us about brain structures underlying the coordination of transport and grasp components of reaching? As noted in the Reach and grasp section, Principle 1, hemiparetic stroke patients have decits in arm movement when reaching, but they are usually more affected distally, so that hand shaping is particularly disrupted. Hermsdorfer and colleagues have contrasted the effects of left and right brain damage on reach and grasp actions. Their interest was not in the effects of hemiparesis per se, indeed they asked participants to use the limb ipsilateral to the lesion, but rather in the possibility of differential contributions to the organisation of action exerted by left and
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right cortical regions. In one study (Hermsdorfer, Ulrich, Marquardt et al., 1999a) they found participants with right brain damage (RBD) were more impaired in nal approach to a target object that was to be lifted, while those with left brain damage (LBD) exhibited greater incoordination. However, both groups exhibited preserved scaling of movements to objects size and distance. In a second study (Hermsdorfer, Laimgruber, Kerkhoff et al., 1999b) the task was made more complex; a cylinder which was resting in different orientations (cf. the task described by Rosenbaum et al., 1990, Rosenbaum et al., 1992) had to be grasped and placed in a hole. When choice of grasp on the bar was constrained, patients with LBD were more impaired, when the grasp position on the bar was free, RBD patients were more impaired. A correlational analysis indicated that these decits were independent of apraxia or visuospatial impairment. Reach to grasp has also been studied in cerebellar patients. A case study of impaired reaching in a cerebellar patient was reported by Haggard, Jenner and Wing (1994). Ataxic movement in reaching with the involved side contrasted with smooth straight-line reaching with the other hand. The hand on the affected side opened wider and also opened earlier than on the unaffected side. Rand, Shimansky, Stelmach et al. (2000) evaluated reach to grasp actions carried out by a group of patients with cerebellar ataxia. They conrmed the increased aperture in reaching and also observed greatly increased variability of timing of the phases of reaching in cerebellar patients. Impairments observed in reaching for objects by parkinsonian patients suggest a contribution of the basal ganglia to the sequential organisation of transport and grasp. Castiello, Stelmach and Lieberman (1993) assessed the reach to grasp movement of eight patients with Parkinsons disease and eight controls. Participants reached between 15 and 40 cm for a small (0.7 cm) or a large (8 cm) diameter dowel. There were no differences between the two groups of participants in their regulation of movement parameters relating to changes in object distance or size. However, in Parkinsons disease patients, the onset of hand closure was delayed with respect to the onset of transport. The authors suggested that this reects a decit in the simultaneous or sequential implemen94
tation of different segments of a complex movement. Alberts, Saling, Adler and Stelmach (2000) observed increased variability in the point at which aperture began to close, as well as disrupted coordination of transport and grasp in patients with Parkinsons disease. They suggested that basal-ganglia dysfunction affects the specication of movement parameters used to produce a consistent pattern of coordination between prehensile components. The results of these studies are consistent with an earlier report of impaired handarm coordination. Benecke, Rothwell, Dick et al. (1987) compared the performance of normal controls and Parkinsons patients in a set of tasks in which participants made scissor-like movements of the hand, moved the hand to a target or combined the two movements in a sequence. While the parkinsonian group performed the isolated tasks slower than controls, they were further impaired in sequencing the two movements leaving an additional delay between the two components. Implications for rehabilitation Assessment. The Fugl-Meyer assessment includes items related to hand function but these take the hand in isolation. Given the principle of handarm coordination set out in this section, we advocate an evaluation that includes the effects of reaching for a standard set of objects at a range of distances, orientations and directions. Observation of handarm coordination is challenging to the naked eye, so that video-recording is advantageous. Training. In considering retraining of coordinated function of the hand and arm after stroke hemiparesis, we have already noted that hand function is usually compromised to a greater degree than arm function. Typically, hand function after stroke is limited to whole-hand movements without differentiated nger movement (Lang and Schieber, 2002; Twitchell, 1951), so one issue is how might hand function be restored. One approach might be to work on hand in isolation. However, again, given our principle, it may be more productive to put hand function in a reaching context. So training might involve reaching for objects with support for the weight of the arm provided at the hand as necessary. Hand support might, in addition, include assistance with shaping the hand. A relevant animal study in this area was
conducted by Nudo et al. (1996). After small unilateral lesions of the hand area in the primate motor cortex, animals were left with palmar grasp based on undifferentiated movement of the ngers. However, the animals recovered a considerable degree of their previous dexterity when provided with practice, retrieving food placed in progressively smaller wells requiring increasing differentiated movements of the digits. So it might be productive to develop a therapy approach based on working with a set of real objects whose manipulation requires progressively more individuated nger movement may work (Ada, Canning, Carr et al., 1994; van Vliet and Turton, 2001). What other elements for training of reach and grasp actions can be identied with the principle of coordinated armhand function with visual guidance? First, the parallel control of reach and grasp suggests that pre-grasp and grasp control is best recruited in the context of a reaching action rather than in isolation. Second, the importance of visuomotor control of reaching indicates that the presence of a real object (as target) is better than an imaginary or nonexistent object during training (Wu et al., 2000). Finally, the importance of active touch for object manipulation suggests that the use of familiar objects with well-established expected sensory cues and known semantic properties is better for grasp and manipulation tasks than non-familiar or imaginary objects (Gordon, Westling, Cole and Johansson, 1993; Jeannerod et al., 1995). Thus, we propose that, when practice is designed in the context of these real motor or environmental problems, the damaged nervous system is more likely to recognise the task and respond through ecologically valid control strategies (see also Ma, Trombly and Robinson-Podolski, 1999). In spite of the lack of any direct evidence, there are several lines of indirect evidence that support our suggestion as to the importance of the task context in neurorehabilitation. First, a recent metaanalysis of 17 studies compared outcomes from occupationally embedded exercise programs with rote exercise (i.e., exercise done for its own sake) programs (Lin, Wu, Tickle-Degnen and Coster, 1997). The benets of participation in purposeful activity compared to movement per se were evidenced in better quality of movement (Lin et al., 1997; Nel-
son, Konosky, Fleharty et al., 1996). It seems that functional signicance and meaningfulness of the task invokes the engagement of ecologically valid movement strategies for participation. The second line of evidence to support the importance of meaningful tasks in rehabilitation is suggested by the way in which the nervous system is organised to perform the visuomotor transformation for reaching and grasping actions (Jeannerod et al., 1995). As we noted earlier, there is a perceptionaction distinction in the use of vision which corresponds to ventraldorsal processing streams (Goodale and Milner, 1992). Object attributes (size, shape) are processed differently depending on the task. If the task is action-oriented, object attributes are processed for function-generation of the appropriate motor commands for reaching and grasping. In contrast, if the task is perception-oriented, object attributes are processed to invoke a specic percept (i.e., object identication, object affordance, etc.). While these two tasks reect very different cognitive functions, they can and do inuence each other as evidenced by the case of AT who had a lesion affecting the pragmatic dorsal-action stream but not the semantic ventral-perception stream. AT could not preshape her grasp when reaching for neutral, unfamiliar objects such as a plastic cylinder, but when reaching to grasp an object with familiar semantic properties such as a lipstick, she demonstrated normal preshaping and reasonable accuracy (Jeannerod et al., 1995). This latter example demonstrates the powerful therapeutic benets of task practice that involves meaningful, purposeful and familiar activities. Another important implication of separate visual routes for perception and action is that use of conscious delayed processing may add an extra drive to benet action. For example, Gentilucci, Benuzzi, Bertolani et al. (2000) showed that verbal labels have an effect on the kinematics of reaching in normal participants. Thus the word small or large printed on the object inuenced maximum grasp size. In cases where there is a failure to use vision to drive action based on retrieved object memories, verbal labels might be substituted, in a sense using language as a second route to action. If language can provide redundancy to aid action, so there may be redundancy within visual cues which may also help drive action. This point is illustrated by another study by
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Gentilucci (2002). He asked participants to pick up objects which varied in properties such as overall size, etc., but the grasp point was of constant width. He found that the grasp kinematics (e.g., maximum aperture) was affected by other features of the object which were not strictly relevant to the dimensions of the grasp position. This suggests that training should include a variety of objects not just different sizes of the same object because we do not know which visual cues may be effective. This strategy is also supported by the variability of practice learning principle (see section Common ground and implications for rehabilitation below). Finally, there has been some attempt to exploit the existence of visually triggered inherent movement repertoires (an inherent vocabulary) for rehabilitation with mirror therapy. Using a mirror positioned in the parasagittal plane, Ramachandran and others have induced synaesthesia in phantom limbs (Ramachandran and Rogers-Ramachandran, 1996), attempted to alleviate visual hemineglect (Ramachandran, Altschuler, Stone et al., 1999), and provided illusory visual feedback of movement for rehabilitation of hemiparetic patients (Altschuler, Wisdom, Stone et al., 1999; Sathian, Greenspan and Wolf, 2000). For the moment, these ndings are limited and currently restricted to a small numbers of subjects. Much more work is needed in this area for a fuller understanding of how this approach might facilitate recovery in cases of central paresis. The idea is that the impaired pathways receive input (are cued) by the cues for mirror symmetric movement (see Principle 1 in the Bilateral movements section). Principle 3: Object manipulation involves a mix of feedback (reactive) and feedforward (predictive) control Our earlier tea-making scenario included several examples of picking up various objects. Precision grip, in which the sides of an object are held between one or more ngers and opposing thumb, is a versatile means of holding an object. Grip force developed at right angles (normal) to the surface, when combined with surface friction, permits force to be developed along (tangential to) the grasp surfaces. This frictional force, which increases in proportion to the
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normal grip force, means that the arm can apply a vertical lift force sufcient to overcome load force due to the weight of an object, and so lift it from a support surface. Once the object is in the air, if the arm applies horizontal force, the tangential frictional force can overcome the objects inertia, allowing it to be accelerated in the direction of the force provided by the arm. A number of studies of lifting and moving familiar objects have shown that grip force rises with or slightly ahead of, and hence predicts, load force. By contrast, if load force changes unpredictably, perhaps because object weight is altered unexpectedly, or because an unknown external force acts on the object in addition to gravity, grip force is adjusted in reaction to (and hence follows) the load force change. The principle we propose here is that both feedforward and feedback mechanisms are fundamental to movement control. In this section we review research on reactive and predictive control of handarm coordination in grasping and manipulating objects. Empirical evidence Empirical evidence for a mix of reactive and predictive control in upper limb movements comes from studies of the coordination of hand and arm movements in the use of stable grasp to hold objects when lifting them up and moving them around. When holding an object with at vertical sides between thumb and nger, the grip force normal to the surface is adjusted to the frictional conditions between the digits and the object surfaces and to the load acting tangentially to the surfaces (Johansson and Westling, 1984). The tangential load at each digit is often just a downward force equal to half (since there are two digits) the weight of the object. If the normal grip force is insufcient, the load force will exceed the tangential frictional force and the object will slide from grasp. The minimum grip force required to prevent this from happening is referred to as the slip force (Westling and Johansson, 1984). People usually adopt a grip force that creates a safety margin (the difference between the grip force and slip force expressed as a percentage of the slip force) of the order of 20%. If a slip begins, for example, when load force is unexpectedly increased (e.g., Johansson and Westling, 1987), grip force increases with a latency of some 80 ms. This latency is considerably in
excess of the 30 ms required for a spinal reex and probably involves supraspinal pathways. In using precision grip to pick an object up (rather than just holding it) the lifting action of the arm generates a load force. As the load force increases, grip force must be sufcient to allow the development of a frictional force that opposes the load, so that the digits do not slide over the surface. Then, once lift force matches object weight, the object rises off the supporting table. Experiments on coordination of grip and load force (the latter indexing the arms lift force) have shown that grip force rises slightly in advance of load force, at every point keeping above the slip force (Johansson and Westling, 1984; for review see Johansson, 1996). This led Johansson and Westling to suggest that control of grip force is based on predicted load force, and not on feedback of the consequences of load force changes, such as increasing shear force or slip at the digits. The grip force required to prevent slip when holding an object increases with its weight. Once subjects are familiar with object weight, Johansson and Westling (1988) observed that the rate of increase of load force is greater with heavier loads. In fact, the time from the start of lifting to object lift-off (the point at which load force matches object weight) is approximately constant over a range of weights. Other factors than load force are important in determining the appropriate level of grip force. For example, a reduction in friction requires greater normal force (Johansson and Westling, 1984). Or, if the load includes a torque term because the object centre of mass is displaced from the grip axis between thumb and index nger (Goodwin, Jenmalm and Johansson, 1998; Wing and Lederman, 1998), greater normal force is required to prevent the object rotating in the grasp. In these cases, as with increases in object weight, when a larger increase in grip force is required and the subject is familiar with the conditions, the rate of increase of grip force is adjusted. Thus the timing of the action remains constant. Such constancy of timing is exploited by the CNS. For instance, Johansson and Westling (1987) showed that lift-off is reliably associated with a burst of activity in afferent bres identied with Pacinian receptors having rapidly adapting, large receptive elds. If the timing of this event is different from expected, for example, if the afferent burst occurs
early because the weight is less than expected, sensorimotor memories for the action may be updated so that action will be better adapted to conditions on the next occasion. A similar exploitation of timing constancy for feedback processing may also underlie the observation of constant time taken to reach for objects at different distances (Jeannerod, 1984). In this case timing constancy is achieved by increasing velocity with reach distance. The expected sensory event here may be contact with the object and an error in timing might be the basis for recalibrating perceived distance. In lifting, when load conditions are not as expected and feedback results in a reactive adjustment, it is important to note that the correction is scaled to do more than just remove the error at the time at which it occurred. Thus, reex corrections to grip force have a predictive aspect in that they allow catch-up of the load force (Johansson, Hger and Bckstrm, 1992a, Johansson, Hger and Riso, 1992b, Johansson, Riso, Hger and Bckstrm, 1992c). Moreover, the reex response is adapted to context in that the response depends on possible or previously occurring errors (Ohki, Edin and Johansson, 2002). The goal of picking up an object is usually to move it. Forces generated by the arm are used to accelerate and then decelerate the object to take it to its new position. The digits constitute the mechanical interface through which the forces are used to overcome the inertia of the object to achieve the accelerations (Fig. 5). Consider a horizontal movement; load forces at the digit rst rise as the object is accelerated, then rise again (but now in the opposite direction) as the object is decelerated and brought to rest. We noted earlier that the grip force used to hold an object in a static position has a safety margin of some 20% above the minimum required to prevent slip due to gravity. The increase in load force during horizontal movement easily exceeds this and so adjustments to grip force are required. Flanagan (1993, 1994) (for review see Wing, 1996) demonstrated that such adjustments are made in parallel with load force changes, with strong positive correlations in timing and amplitude between peaks in grip force and load force. Moreover, in vertical movements they showed that the peak in grip force moves systematically earlier or later depending on whether the load force
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Desired state

Muscle command End state
Inverse model
Sensory based correction Sensory prediction
Effector
Efference copy
Forward dynamic model Forward output model

Corollary discharge
Sensor
Reafference
Sensory discrepancy
Fig. 5. Schematic representation of inverse and forward models for the control of movement.
rises early, in upward movements, or later, in downward movements. Thus, in moving up, the inertial load force due to acceleration sums with gravity to produce an initial increase in load force. In contrast, in moving down, the hand acceleration typically matches gravity and there is an initial reduction in load force (relative to the hand, the object becomes momentarily weightless) and load force only rises towards the end of movement as deceleration introduces forces opposing gravity. Flanagan and Wing (1997) argued that the parallel changes in grip and load force suggest that the CNS uses information about the consequences of moving on which to base a prediction of load force and thus make anticipatory adjustments to grip force. One way of doing this is to take the commands to the arm muscles and use an internal model of the effector kinematics and dynamics to determine what load force will arise. This model, which is termed a forward model because it takes motor commands as input and estimates the resulting dynamics and kinematics, contrasts with the so-called inverse model, in which motor commands are determined given effector kinematics and dynamics as input. In order for the forward model to determine the outcome of motor commands it is necessary to know the physical characteristics, not only of the effector system, but also of the object. The most obvious object characteristic is the mass (as already noted). Another important characteristic is the distribution
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of mass. In precision grip, if the grip axis formed by the line between index nger and thumb does not include the centre of mass, the load force through the centre of mass will produce a turning force, or torque, at the digits. It has been shown that anticipatory adjustments to grip force take account of such torque loads (Jenmalam et al., 1998; Wing and Lederman, 1998). Interestingly, such information is local and does not appear to transfer between the hands. Thus, Salimi, Hollender, Frazier and Gordon (2000) showed that learned predictive adjustments to individual nger lift forces to achieve level lifting of an object with off-set centre of mass did not transfer when the other hand was used to lift the object. Learning and development The development of precision grip in anticipatory control of lifting has been described by Forssberg, Eliasson, Kinoshota et al. (1991) and Forssberg, Kinoshota, Eliasson et al. (1992). Children and adults repeatedly lifted a small object between thumb and index nger. Compared to the smooth increase of grip force with load force evident in adults, children under the age of 2 years exhibited prolonged preload phase (rise in grip before rise in load force) and a load phase in which grip and load forces did not increase in parallel. In older children the preload and load phases became more adult-like. However, the bell-shaped single-peaked force proles of adults were only becoming evident in older children aged
8 and above, indicating the emergence of an anticipatory strategy and less reliance on the feedback control of the early years. In a further study Forssberg, Eliasson, Kinoshota et al. (1995) examined the adaptation of grip forces to the frictional conditions. They noted that the youngest children (18 months) used much higher grip forces even with high friction (sandpaper) grasp surfaces. In order to adapt grip force to different surfaces, younger children required a greater number of repeated trials with the surface. The authors suggested that this reected a reduced capacity in younger children to form a sensorimotor memory representation of the friction or else a poor capacity to control the appropriate force ratio based on that representation. In contrast, older children required only a few lifts and adults only a single lift to update their force coordination to a new surface with changed friction. The work of Forssberg and colleagues emphasises continuing development in the anticipatory control of grip force over the rst 8 to 10 years. Perhaps surprisingly, Blank, Breitenbach, Nitschke et al. (2001) found that, in terms of temporal coupling, grip force modulation with cyclic load force uctuations above 1 Hz (due to repetitive up and down movements of the hand held object) was as well developed in children aged 4 years and over as it was in adults (see Flanagan and Wing, 1995). For the low frequencies (less than 1 Hz) children in all age groups (36 years) exhibited small but reliable increases in the phase lag between load and grip force. In contrast to the tight coupling in timing, children showed much less tight coupling between the grip force and load force. The authors concluded that the differential development of temporal and gain control reects a contrast between contributions of earlier maturing cerebellar temporal functions and later developing cortical control over force amplitudes. The idea of a forward model, used to predict movement consequences on the basis of motor commands, assumes a means of generating motor commands on the basis of desired movement in the rst place. How might such an inverse model be acquired? One proposal is that it might be learned using feedback error correction as a training signal (Kawato and Gomi, 1992). Consider lifting an object. An inverse model is required to specify the required muscle commands to grip the object stably
during lifting. Suppose, initially, that an inaccurate inverse model is used and grip force is insufcient. As the arm develops lift force, a slip will occur and this will trigger a fast feedback loop to increase grip force. The motor command to achieve this correction may also be used to adjust the inverse model so that, in future, the task of lifting the particular object will elicit a greater grip force under the inverse model. Such an approach will work provided that a feedback error correction exists in the rst place. Learning is complete when the inverse model results in goal attainment without any need for feedback error correction. There is evidence for such feedback error learning of the inverse model based on cerebellar circuits in the case of eye movements (Wolpert, Miall and Kawato, 1998). In the next section we review a brain activation study supporting the involvement of the cerebellum in learning upper limb movement. Feedback or feedforward control of action requires sensory information about the effector system as well as about the target. Information about the target may come from vision, either directly (for example size, shape) as discussed in the previous section (Principle 2 Reach and grasp), or from visual cues to memory. Thus Gordon et al. (1993) reported that load force rates are scaled to familiar objects with different weights so that the lifting the various objects took approximately the same time. Information about the effector system is available form tactile and proprioceptive systems. Loss of sensory input results in failure to adapt to unpredictable load increases (Johansson et al., 1992a). However, in cyclic voluntary movement, timing between load and grip force is preserved (Augurelle, Smith, Lejeune and Thonnard, 2003; Nowak, Hermsdorfer, Glasauer et al., 2001). Neural basis Single-unit studies have provided important information about the neural bases of reactive and predictive aspects of motor control. For example, Smith and colleagues trained monkeys to lift and hold instrumented objects using precision grip to study the coordination of load and grip forces. In one study (Brochier, Boudreau, Pare and Smith, 1999) muscimol was used to inactivate small regions of motor (MI) and somatosensory (SI) cortex. Lesions in MI impaired independent nger movements, and caused reduction in force levels in precision grip used in
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lifting. Lesions in SI produced incoordination of grip force and load force and grip force was overall elevated, perhaps as strategic compensation. This clearly demonstrates the importance of sensory input even in the predictable loading associated with voluntary lifting. Another study from the same lab (Salimi, Brochier and Smith, 1999a) examined neuronal activity in SI in lifting. The majority of the receptive elds observed were cutaneous and covered less than one digit. Three broad categories of discharge pattern cells were identied. Dynamic cells, showed a brief increase in activity beginning near grip onset. Some of these neurons responded to both skin indentation and release. Static cells, had higher, sustained activity during the stationary holding phase of the task and demonstrated varying degrees of sensitivity to rates of pressure change on the skin. The third category comprised cells with signicant pre-grip activity and included cortical cells with both dynamic or static discharge patterns at grip onset. Cells in this category showed activity increases before movement in the absence of receptive-eld stimulation, suggesting that, in addition to peripheral cutaneous input, these cells also receive strong excitation from movement-related regions of the brain. It may be that these cells are tuned to the predictable elements of lifting and have a special role to play if the afferent input during lifting unexpectedly departs from the normal pattern. A further study explored the dependence of SI activity on weight and surface texture of the object being lifted (Salimi, Brochier and Smith, 1999b). In this study an increase in weight or a change to smoother surface texture with lower friction were both associated with higher grip force. Corresponding to the behavioural change in grip force, increases in ring rate were seen in both static and dynamic cells, especially in the case of smoother texture. Some cells responded to texture independent of weight, but no cells were found to be responsive only to weight. Cells with texture-related but weight-independent activities encoded surface characteristics that were largely independent of the grip and lifting forces used to manipulate the object. The authors noted that such constancies would be useful for constructing an internal representation or mental model of an object in order to plan and control its manipulation. Recently, Boudreau, Brochier, Pare
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and Smith (2001) reported on unit activity in premotor areas when an object was lifted and when it was subject to perturbation during the hold phase some 1500 ms after lifting. Cells whose activity anticipated lifting were found in both dorsal and ventral premotor areas, with more in PMd. In both areas, some of these cells responded to perturbation. In selected blocks of trials a visual stimulus was associated with the perturbation. Although this gave rise to earlier rise in grip force, no anticipatory activity was observed in the premotor cells. In spite of anatomical studies showing strong cerebellothalamo-cortical projections involving premotor cortex, the present study suggests that the cortical premotor areas are not involved in the elaboration of adaptive internal models of handobject dynamics. Brain-imaging studies have shown that the regional blood ow in the cerebellum increases at the beginning of learning new tasks both cognitive and motor and decreases as learning proceeds (for a review see Schmahmann, 2000). This might suggest that the cerebellum is only involved in the early phase of learning. However, arguing on the basis of the multiple internal model of Wolpert and Kawato (1998), Imamizu, Miyauchi, Tamada et al. (2000) suggested another interpretation. When learning to carry out a skill in a new environment, the internal models compete and all receive a copy of the error signal leading to widespread cerebellar activation. One (or just a few) of the pairs learn the new sensorimotor transformation, reducing the error signal, and the level of cerebellar activity will be reduced to just a small region. Imamizu et al. (2000) tested this idea by asking participants to learn to use a mouse with a novel 120-degree rotational transformation. On initial exposure, the rotation resulted in two types of increased activation. The rst involved wide areas of the cerebellum and was proportional to the tracking error. A second region involved an area near the posterior superior ssure which remained active even after learning. The authors identied this area with the acquired internal model of the new transformation, noting that anatomical studies have indicated it receives cortical inputs including connections with parietal (which was noted in the preceding section as active in learning kinematic transformations). Turning to patient studies, Grichting, Hediger, Kaluzny and Wiesendanger (2000) examined proac-
tive and reactive grip force control in chronic hemiparetic patients. The task involved using precision grip to pull out a drawer which could be used to create sudden rises in load force, either by an increase in resistance, either during the pulling action or during a phase when the drawer was held open. To retain a secure grip on the handle, an increase in grip force was required to be coordinated with increase in pull to match the rise in load force. In normal volunteers Grichting et al. (2000) observed a reactive increase in grip force. Both in the pull and hold phases, the reactive increase in hemiparetic patients was reduced. In some trial blocks the load increase was predictable and, this resulted in a predictive, early rise in grip force. However, the amplitude of this proactive adjustment was reduced in hemiparetic subjects. Thus the weakness in paresis resulted in impairment in anticipatory as well as reactive grip adjustment. A series of studies by Gordon and colleagues has examined the coordination of grip force and load force in children with hemiplegic cerebral palsy. Eliasson, Gordon and Forssberg (1995) examined gripload force coordination during the lift of a small object with the precision grip in children with CP and controls. Children with CP were able to modify their grip force according to friction between the ngertips and the object and could use tactile information for anticipatory control of the forcescaling of the precision grip, but they seemed to need predictable conditions and successive lifts to build up a memory representation of an objects friction. Gordon and Duff (1999) found that hemiplegic CP children took more trials with their affected hand to develop anticipatory GFLF coordination after a change in weight or surface texture. They attributed these effects to impaired sensory representation. Gordon, Charles and Duff (1999) found that sensory information from the non-involved hand was used for anticipatory scaling of isometric force increase during subsequent lifts with the contralateral involved hand. These ndings suggest that the initial lack of anticipatory control usually observed in the involved hand of children with hemiplegic CP is likely to be based on disturbed sensory input. These studies with CP children thus underlie the importance of sensory factors in coordination. In the Reach and grasp section we have seen that cerebellar damage leads to impaired interjoint
coordination (Principle 1) and impaired coordination in reach and grasp (Principle 2). Several studies have shown that grip and load force coordination are impaired in cerebellar patients. Muller and Dichgans (1994a) used a precision grip task to test two patients with acute unilateral cerebellar lesions due to a stroke and to compare performance of the affected and the unaffected hand. Their results showed that grip force development was slowed and coordination of grip and lift force impaired by the lesion. In a further paper Muller and Dichgans (1994b) examined 21 patients, mostly with degenerative cerebellar disorders, and 10 healthy controls lifting various loads with precision grip. The results showed that cerebellar patients adapted their grip force levels to the different object loads but with a longer latency between the onset of grip force and load force than controls and with a grip force prole with a more irregular pattern, suggestive of a lack of sufcient anticipatory parameterisation. In cerebellar patients the level of pinch force at the start of lift force was elevated. Patients adapted their grip force to different weights based on previous experience through repetitive testing, but were signicantly less efcient in doing this than healthy controls. Cerebellar patients exhibit abnormal gripload force coordination in moving objects, As noted earlier, moving an object results in uctuating inertial load force which is, in principle, predictable as it is proportional to the acceleration and deceleration used in moving the object. Babbe Ratin et al. (EBR) found elevated GF in the affected hand of cerebellar patients in upward and downward vertical movements. Elevated grip force in cases of cerebellar atrophy was described by Nowak, Hermsdorfer, Marquardt and Fuchs (2002). These authors noted impairments of temporal grip force regulation occurring with increasing degrees of dysfunction during the progression of cerebellar atrophy. Serrien and Wiesendanger (1999) used the drawer-pull task described earlier to examine effects of unilateral cerebellar lesions on anticipatory and reactive grip. In the study they compared grip force regulation for the affected and unaffected hand. Again there were two types of perturbation: (1) a brief load perturbation during a self-stopped drawer pull, and (2) a loading impact when the drawer was pulled out to the mechanical stop. The results showed that when a
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self-stopped movement was perturbed during its trajectory, anticipatory grip force increase was smaller for the affected than for the unaffected hand, illustrating a disturbed gain control due to cerebellar dysfunction. When the mechanical stop arrested the movement, the amount of grip force did not differ signicantly between the affected and unaffected side; however, both hands used different control strategies. Whereas the unaffected hand anticipated the load perturbation by a ramp-like increase of grip force toward the impending impact, the affected hand increased grip force at movement onset to a default level and maintained this value until the task was ended. In addition, the latency between impact and reactive peak in grip farce was prolonged for the affected hand, suggesting a delayed cerebellar transmission of reactive responses. In conclusion these ndings demonstrate that the cerebellum is involved in anticipatory and reactive mechanisms dealing with load perturbations during goal-directed behaviour. In contrast to the effects of cerebellar disease on coordination of grip and load force, studies of object manipulation in patients with Parkinsons disease suggests abnormalities in grip force control during lifting (Forssberg, Ingvarsson, Iwasaki et al., 2000; Ingvarsson, Gordon and Forssberg, 1997) or moving (Nowak and Hermsdorfer, 2002) an object can be related to tremor. Implications for rehabilitation Assessment. Since movement control involves a mix of feedback and feedforward control both forms of control should be assessed. Thus the use of grip force in holding an object might be evaluated under conditions where the load force is either predictable (due to voluntary movement) or unpredictable (due to a change produced by the experimenter). The FuglMeyer Tests include assessing grip (pen top between thumb and index nger). A useful addition might be to include assessment of the predictive development of grip in picking up objects of varying weight. If a styrofoam cup is used with varying weights in the cup, the bending of the cup could provide a useful visual cue to the grip force being employed. A further useful test would be to assess reactive grip force. This might involve holding the same cup with eyes closed while the assessor provides an abrupt upward push at an unpredictable time from below.
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Treatment. Based on the principle that normal movement involves a mix of feedback and predictive control, a rehabilitation programme should include both these elements. Thus, a training exercise might include a phase in which a functional posture (e.g., hand holding out a cup) is held against unpredictable perturbing forces, but this should be followed by a phase in which the perturbation is made predictable in time and space. This might involve repetition of the perturbation under similar conditions. Or it might be a case of providing advance warning of the upcoming perturbation in terms of visual cues (drawing on memory for familiar objects. Thus, a small, light or large, heavy object might be dropped into the cup) and or verbal cues (development of appropriate predictive grip for an object dropped into the cup might be improved if the label light or heavy is given as the object is dropped to enlist semantic routes to action). The move from feedback-driven to predictive action, started with giving advance cues to the perturbation could be further developed by playing a game in which the cup is moved to throw the object up and then catch it again with the cup. This could be carried out in a cyclic manner which would encourage stable patterns of coordination between load force created by the action and grip force (Augurelle et al., 2003; Nowak et al., 2002). This might be combined with an auditory pacing stimulus to encourage regularity of movement which has been shown in simple aiming to be benecial to motor coordination in patient groups (Thaut et al., 2002). The importance of the cerebellum in prediction has been noted. It might therefore be thought that patients with cerebellar decits might particularly benet from practice in prediction. Lang and Bastian (1999) studied cerebellar prediction in keeping the hand in a xed position when catching balls dropped from above the hand. In one study subjects were exposed to a series of light balls which were then switched to a series of heavier balls. Compared to normal controls, the cerebellar group adapted very slowly to the changed conditions. In another study Lang and Bastian (2001) examined whether prior or on-line information about ball weight and drop height could improve the impaired adaptation of people with cerebellar damage. Cerebellar and control subjects caught a series of balls of different weights under two conditions. The rst condition provided
subjects with information about ball weight prior to the series of trials. The second condition provided subjects with information about ball weight, drop height, and time of ball release during the series of trials. Subjects again had to maintain their hand position within a vertical spatial window. With prior information, controls required a few trials to adapt to a new ball weight. Cerebellar subjects were slow, or unable, to adapt. With on-line information, controls were able to catch the ball within the window immediately, showing that they did not require practice to make this adjustment. Cerebellar subjects remained slow or unable to adapt to the changed ball weight even with on-line information. These results suggest that other, intact central nervous system structures cannot compensate for the role of the cerebellum in generating and adjusting anticipatory muscle activity across multiple joints. However, the effect of long-term training was not assessed. Reach and grasp summary We have now presented three principles for singlehand movement. Under the rst principle, we described the coordination of shoulder, elbow and wrist movements underlying straight-line hand paths, arguing that the CNS represents actions in terms of hand path. We also considered possible benets of representing arm movements in hand space when reaching to for objects in the environment. Under the second principle we treated multiple sensory routes to action with illustrations from handarm coordination in reaching to grasp. We used the control of grip force to illustrate the third principle that complementary reactive, feedback and predictive, feedforward mechanisms contribute to coordination of nger and arm actions. Bilateral movements Reaching, grasping and lifting a tea cup require a sophisticated unilateral action as we have seen above. If, instead, you reach for a biscuit at the same time as your teacup, the motor control necessary to accomplish these tasks contains an additional element or problem to solve, that of coordinating the two limbs together as they do variations of the same task. Later on, you might also need to brush crumbs off your lap
using repetitive actions with both arms. You will also need to stir or drink your tea while holding a saucer steady with the other hand. The motor control of bimanual movements such as the above scenarios can be encapsulated in the following three principles: (1) under task situations requiring simultaneous movements, the arms are coupled together as a unit; (2) in continuously repetitive tasks, the arms entrain to only two stable coordination states, moving together (mirror symmetric or in-phase) and moving in opposition (anti-phase); (3) each hand is specialised for different functions within non-symmetrical bimanual tasks. These principles are not independent of each other or of those for unimanual tasks; and for the purposes of explanation and discussion they are presented such that principles 2 and 3 elaborate on the fundamental principle 1. Principle 1: Under task situations requiring simultaneous movements, the arms are coupled as a unit In tasks where the hands function simultaneously, such as reaching for two things at once, the spatial temporal relationships of each arm are tightly coupled together. When the hands do exactly the same task the coupling is stronger but particularly when the hands are doing different aspects of a task, bimanual control is seen to be shared or, put another way, under one control regimen demonstrating interlimb coupling. Specically, the spatialtemporal relationship of each arm in the corresponding unilateral task is altered in the bimanual case. Empirical evidence For example, the movement of one hand quickly between two targets on a table is accurately described by Fitts law that accounts for the speed accuracy relationship (Fitts, 1954) (Fig. 6). If the other hand moves at the same time but to a different distance, Fitts law no longer applies as the hands are temporally coupled to arrive at their respective targets together (Kelso, Southard and Goodman, 1979a; Kelso, Southard and Goodman, 1979b; Kelso, Putnam and Goodman, 1983). Furthermore, placing an obstruction in the path of one hand results in, not only a maintenance of the temporal coupling, but also a demonstration of spatial cou103
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OBSTACLE
Home Keys
TARGET 1
TARGET 2
Fig. 6. Schematic representation of the tendency for hands moving from home keys to targets of different distances to arrive at the same time (duration t ) as in temporal coupling and to show a spatial coupling with hand without an obstacle in the path being inuenced by the hand that moves over the obstacle as in spatial coupling.
pling as the non-obstructed hand detours in a similar, but lower-amplitude path as the obstructed hand (see Fig. 5). Similar results are found in more functional tasks of bilateral reaching and grasping (Jackson, Jackson and Kritikos, 1999). In these examples, the arms have different parameters (e.g., amplitude) of the same task. If, instead, the hands have different functions, for example, one pulling a drawer open and the other reaching inside for an object (a quasi-sequential task) the hands are still synchronised and correlated to begin and end their respective tasks as one temporal unit (Perrig, Kazennikov and Wiesendanger, 1999). These data suggest coupling mechanisms that the central nervous system exploits that reduce the complexity of organising two tasks by controlling them as a single unit often referred to as a coordinative structure (Tuller, Turvey and Fitch, 1982). Complementary ndings at the level of force control are found in investigations of grip forceload force coupling, where grip force is the force necessary to hold an object between two ngers and load force is the force necessary to move the object (see Principle 3 in Reach and grasp section). During unimanual and bimanual symmetrical movements of lifting a weight, there is an automatic increase in grip forceload force ratio for long versus short amplitudes as well as for light versus heavy weight movements. During asymmetrical movements where parameters of weight or distance are manipulated, the grip forceload force ratio is comparable for both sides suggesting that a bimanual control mechanism overrides the automatic grip forceload force coupling (Serrien and Wiesendanger, 2001a). Again, the same principle holds for different functional
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tasks. If one hand holds an object statically while the other opens a drawer, the grip forceload force ratio of the former is shifted towards the latter (Serrien and Wiesendanger, 2001b). This suggests rst that dynamic activity exerts a greater coupling force on static activity, perhaps through attentional focus. Second, since the increased force ratio was restricted to grip and not load force (which remained constant) and since grip and load commonly co-vary during a manipulative action this again reinforces the idea that bimanual control overrides unimanual instantiated relationships. Taken together, these experiments suggest that bimanual actions are achieved by an overriding unitary coordinative structure that simplies control. That this control exists at multiple levels of organisation is suggested by its generality to temporalspatial and force output as well as to the differential parameterisation of one task and to two different functional tasks. The ubiquity of bilateral synchronisation is striking. We now consider whether it is immutable either developmentally or in terms of learning to overcome the synchronisation since this will have implications for mechanisms as well as for rehabilitation. Development and learning The appearance of bilateral synchronisation occurs gradually during infancy and early childhood. At birth, a primitive form of symmetrical bilateral coordination is present in some reexes (e.g., Moro or Symmetric Tonic Neck Reex) but these neural pathways are transient and do not appear to be a direct precursor to voluntary bimanual coordination (see Fagard, 1994). Instead, bilateral coordination appears to develop from the repetition
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of spontaneous arm movements and accompanying neural changes. Using a technique of correlating the acceleration and deceleration of spontaneous arm movements, Thelen and colleagues (Corbetta and Thelen, 1994; Thelen, Corbetta, Kamm et al., 1993) demonstrate that 5-week infants show few episodes of highly correlated bilateral movement whereas by 1 year spontaneous bilateral movements are highly correlated most of the time. Furthermore, periods of highly correlated bilateral vs. unilateral movements uctuate across the rst year of life in synchrony with periods of predominantly bilateral vs. unilateral reaching. Infants, also, tend to show bilateral movements before unilateral which is consistent with observations that they begin reaching (around 1216 weeks) using two hands symmetrically before attempting unilateral reaches (e.g., Ramsey and Willis, 1984; White, Castle and Held, 1964). Together, these data suggest that motor control is easier initially for bilateral symmetrical than unilateral movement. Regarding bimanual differentiation of function, older infants progress from a sequential (e.g., reach for one toy and then reach for the other) to a more simultaneous form of timing (where initiations of reaching overlap). However, even when infants can coordinate two very dissimilar functions quite well by the second year of life, it is not clear that they have the same kind of tight unitary control over their movements as observed in adults. In a more direct comparison with adult data, Southard (1985) replicated the Kelso task (Kelso et al., 1979a,b) cited above, in children from 5 to 14 years. All ages showed evidence of coupling between the arms when distances to move were different. However, the coupling was not as tight, in terms of temporal coherence, as adults until around 10 years of age. This suggests that ne-tuning of the coupling continues to occur until this age. At the other end of the spectrum, aging produces bimanual decits in synchronisation of the initiation and termination of bilateral movements (Stelmach, Armrhein and Goggin, 1988). As seen in the developmental prole, one consequence of the unitary bimanual coordinative structure is that learning the same task with each hand is much easier than doing two very different tasks. The difculty of combining two different tasks is en-
hanced if they require a different temporal or spatial structure and, therefore, are not intentionally allowed to inuence each other. For example, in the Kelso task, where hands move simultaneously to nonequal distance targets, adults require much practice and attention to be able to achieve arriving at different times and therefore uncoupling the usual tendency to arrive simultaneously. Likewise, the task of moving one arm unidirectionally while the other does a reversal of direction, both in a specied time, is also hard to accomplish (Swinnen, Walter and Shapiro, 1988; Swinnen, Young, Walter and Serrien, 1991). In both the Kelso and Swinnen paradigms, there is a spatiotemporal assimilation such that the arms tend to perform a version of the two tasks that lies between the specied parameters of each. In the Swinnen task, the arm required to do the simple movement tends to mimic the more difcult task, presumably, upon which attention is focused. Interestingly, the uncoupling of the two arm actions required in the Swinnen task is not achieved by practice alone, even though practice can sometimes increase the degree of coupling (Swinnen, Walter, Pauwels et al., 1990). Rather, feedback is required either in the form of knowledge about the movement patterns being produced (knowledge of performance) or knowledge about how correlated the arms are (i.e., a discrete outcome variable or result) or ideally both (Swinnen, Walter, Lee and Serrien, 1993). Another successful strategy, termed adaptive tuning, used to aid learning this particular task was to slow the task down and gradually increase it to the criterion speed (Walter and Swinnen, 1992). Both speed (Swinnen, Walter, Serrien and Vandendriessche, 1992) and torque (Walter and Swinnen, 1990a) are related to the coupling tendency in this task in the sense that decreasing either leads to less attraction to the preferred symmetrical state. Thus for learning tasks that require an uncoupling of the symmetrical bimanual coordinative structure, both feedback and adaptive tuning along with practice appear to be necessary. Fortunately, a temporal requirement is rarely specied for a bimanual functional task of daily living and therefore any spatial or force differentiation between the hands can be accommodated without trying to uncouple the hands and/or by slowing the movements down. We now consider the neural basis of this bilateral coupling constraint.
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Neural basis The neural basis of this unied bimanual coordination has been examined using a variety of methods including clinical observations and increasingly sophisticated functional imaging of humans and physiological recordings in animals. Recent reviews suggest that bimanual coordination has a diffuse and distributed basis involving both cortical and subcortical areas (Cardoso de Oliveira, 2002; Wiesendanger and Serrien, 2001). Cortical areas involved include the primary motor cortex where the traditional view of contralateral motor control from each hemisphere has given way to the view that motor control is more shared with overlapping representations of both arms in each hemisphere (e.g., Brinkman and Kuypers, 1972; Chen, Cohen and Hallett, 1997). Bimanual-specic activity has been recorded in M1 via functional magnetic resonance imaging in humans (Toyokura, Muro, Komiya and Obara, 1999) and single-neuron recordings in monkeys (Donchin, Gribova, Steinberg et al., 1998; Donchin, Steinberg, Gribova et al., 2001; Kermadi, Liu and Rouiller, 2000). In addition, there is evidence that the left hemisphere in right-handers (and possibly many left handers too) controls the initiation and termination of movements from both hands (Kimura, 1977; Peters, 1994). For example, the left hemisphere shows greater activation during bimanual movement and a marked change in pattern from the unilateral case compared to the right hemisphere that has less activation and is not sensitive to task changes (Jancke, Peters, Schlaug et al., 1998). Premotor areas also strongly implicated in bimanual coordination are the supplementary motor area (Jancke, Peters, Himmelbach et al., 2000a; Kermadi et al., 2000; Lang, Obrig, Lindinger et al., 1990; Wiesendanger, Rouiller, Kazennikov and Perrig, 1996) and the cingulate cortex area (Debaere, Swinnen, Beatse et al., 2001; Stephan, Binkofski, Halsband et al., 1999) where neuronal activity is enhanced in bimanual rhythmic tasks and particularly so in those that are more complex. The unied coupling observed, then, may be achieved by known bilateral connections (both direct and indirect) from higher-level motor and premotor cortical areas to the spinal cord (Wiesendanger, Wicki and Rouiller, 1994). Lower-level coupling is assumed to occur via indirect pathways such as the ipsilateral
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corticospinal pathways with the idea being that if these pathways carry different movement plans than the direct contralateral corticospinal pathways, some crosstalk may occur. In addition to the evidence that the left hemisphere controls sequencing of actions in both arms, more direct evidence of higher-level coupling via interhemispheric pathways between the cortices has been investigated through patients with surgical lesions of the corpus callosum connecting the two hemispheres. In general, these patients seem to preserve temporal coupling of movements while interlimb spatial coupling interference is no longer present (Franz, Zelaznik and McCabe, 1991; Franz, Eliassen, Ivry and Gazzaniga, 1996). For example, callosotomy patients nd drawing three sides of a square equally easy whether the two hands move symmetrically or orthogonally to one another whereas control subjects nd the latter more difcult. However, the temporal aspects of the tasks are closely synchronised for both groups. These results suggest that spatial coupling involves interhemispheric communication via the corpus callosum while temporal coupling has a subcortical locus. Moreover, the corpus callosum appears to be important for learning new bimanual skills but not in performing old well-learned bimanual skills that can be accessed without callosal connections (Franz, Waldie and Smith, 2000; Preilowski, 1972). A recent review concludes that interhemispheric interaction is particularly important in the initial stages of acquiring a novel bimanual skill (Gerloff and Andres, 2002). The developmental observation that ne-tuning of temporal coupling occurs around 10 years of age is also consistent with the development of the corpus callosum, which is largely (but not totally) complete around the same age (Keshevan, Diwadkar, DeBellis et al., 2002). A coupling role for lower-level circuits including the cerebellum, the brain stem and propriospinal networks has also been proposed (Wiesendanger et al., 1994). For example, the basal ganglia are implicated because patients with Parkinsons disease (Serrien, Steyvers, Debaere et al., 2000; Swinnen, Van Langendonk, Verschueren et al., 1997) and Huntingtons disease (Brown, Jahanshahi and Marsden, 1993) show disrupted bimanual coordination. Similarly, bimanual coordination decits occur in patients
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with cerebellar damage (Brown et al., 1993). For example, temporal synchronisation at the beginning of simultaneous but dissimilar tasks was disrupted (Serrien and Wiesendanger, 2000). However, during the execution of these tasks, synchronisation increased somewhat suggesting that bilateral processes during the execution of the task are less affected by the cerebellar damage. It is not clear whether the role of either the basal ganglia or the cerebellum is directly related to bimanual coordination or whether it is indirectly implicated via a general disruption of all coordination or complex neural pathway loops involving other directly implicated areas (Cardoso de Oliveira, 2002). The fact that rather similar bimanual decits are found across different patient groups underscores the distributed neural basis of bimanual coordination (Brown et al., 1993). Overall, the neural mechanisms underlying bimanual coordination are still not well understood but the unied coupling is considered most likely to arise from a high level internal model of a task (a common feedforward control mechanism) in premotor motor cortices with coupling via the corpus callosum and updated by feedback in accordance with changing internalexternal constraints. Online adjustments may operate at lower levels including the basal ganglia and cerebellum for ne-tuning of an evolving bimanual action (Wiesendanger and Serrien, 2001). Doing bilateral movements then may facilitate coupling or crosstalk from one hemisphere to the other via a number of mechanisms including the disinhibition of cross callosal, and the activation of ipsilateral corticospinal and other bilateral uncrossed pathways (Mudie and Matyas, 2000). Implications for rehabilitation Assessment. It can be argued that many, if not most, activities of daily living (e.g., washing or dressing) and instrumental activities of daily living (e.g., telephone use or preparing a meal) typically use two arms albeit primarily in complementary and/or serial roles rather than identical, symmetrical roles (see Principle 3 in Bilateral movements section). Thus, it is important to assess bilateral tasks for this reason, alone, even if only one arm appears impaired. Surprisingly, explicit reference or testing of bilateral activities of the hands/arms is not strongly emphasised in standardised assessment scales of daily
use (e.g., Stroke Impact Scale, Duncan, Wallace, Lai et al., 1999) or functional limitation (e.g., Wolf Motor Arm Test, Wolf, Catlin, Ellis et al., 2001). From a conceptual viewpoint, performing two tasks simultaneously may result in less impairment due to the coupling principle discussed above and this was demonstrated in patients with Parkinsons disease (Stelmach and Worringham, 1988) although no advantage either way was found in very high functioning stroke patients (Platz, Bock and Prass, 2001). Treatment. Can patients who have chronic motor performance-related disease or damage to any of the relevant higher or lower levels of the central nervous system relearn any of their bimanual coordination ability? Given that unitary coupling of bilateral actions is a fundamental principle can it be exploited or, in situations where the tendency to couple is too strong, can this be overcome through interhemispheric inhibition. Only the rst question has been studied in patient populations. One positive application of the coupling principle is to harness existing coupling abilities by encouraging bilateral movements to recover function of an involved limb. Thus, in the case of a patient with a unilateral, cortical stroke, forcing the use of both limbs as opposed to the paretic arm only, (as in constraint-induced therapy see section Practice and active participation are fundamental to motor learning) may yield additional benets by accessing intact processes of the non-lesioned hemisphere and the possible neural coupling mechanisms described above. Rose and Winstein (2002) have assessed the temporalspatial coupling of patients with stroke who were asked to move their hands simultaneously or separately in a ballistic goal-related task. In addition to demonstrating clear temporal coupling in the bimanual conditions, they found a facilitation effect in 5 of 11 patients where the involved limb had a shorter movement time in the bimanual condition. In a similar study, Cunningham, Stoykov and Walter (2002) found that 3 of 6 patients showed smoother movements of the involved arm in a bilateral vs. unilateral discrete elbow extension task. In addition, 5 of 6 subjects showed benets of the involved arm when the uninvolved arm was inertially loaded in the bilateral condition compared to the unilateral condition. These studies support the idea that control of the
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involved arm can improve during bimanual performance at least in some patients with hemiparesis. If these effects can be found immediately, what will bilateral training over several sessions provide? In controlled single-case experiments with multiple-baseline designs, Mudie and Matyas (2000) trained 12 patients with unilateral stroke on three standardised reach-to-target tasks. They demonstrated that performing these tasks in simultaneous bilaterally identical but independent movements (bilateral isokinematic training or BIT) produces immediate, clinically and statistically different improvements compared to baseline practice of unilateral, bilateral with non-paretic arm guiding the paretic, and bilateral with arms doing two of the tasks simultaneously. The benet occurs regardless of whether the three tasks are tested and practiced in a random way or whether blocked practice of one is used; and also regardless of the amount of time devoted to each type of training. The authors speculate that BIT promotes interhemispheric disinhibition of cross callosal, indirect and ipsilateral corticospinal pathways from the intact hemisphere that are typically inhibited during unilateral action. These disinhibited pathways might aid in reorganisation by the sharing of normal movement commands. Convincing though the data from Mudie and Matyas are, there are at least four caveats from the study. First, all but one patient was in a subacute phase, some with concurrent rehabilitation. Therefore, confounding factors were present although these should also affect the baseline treatment. Second, since BIT was always second, it is possible that a novelty effect produced extra effort resulting in the immediate improvement seen and, in most subjects, followed by a slight deterioration before stabilising or beginning to improve more gradually. Third, although improvement was maintained during subsequent BIT sessions, no retention data are available so the durability of BIT is not known. Fourth, improvements were measured on the training tasks which, in a single-case design with three different tasks, is not a major issue but there is no attempt to show whether gains were generalised to other related functional tasks or, more importantly, to other bilateral tasks or the top level of the model of rehabilitation. A second intervention experiment featuring bilateral arm training was based on Neurodevelopmental
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Treatment principles. This study did use patients beyond spontaneous recovery, along with a randomised, controlled two-group design, a retention test after no practice and a variety of outcome measures (van der Lee et al., 1999). The comparison was with unilateral constraint-induced therapy. Both groups made minor gains; however, statistically there was a small but lasting effect of constraint-induced therapy on the dexterity of the affected arm and a temporary clinically relevant effect on the amount of use of the affected arm during activities of daily living. This study is notable because it showed that bilateral training, albeit based largely on passive movements, was almost as good as the well-known, successful forced active use of constraint-induced therapy. Criticisms of this study include the highlevel functioning of the patients at the beginning of training which might have engendered a ceiling effect and the lack of detail and control concerning either training protocol. A well-designed and controlled intervention study, which deliberately attempted to harness the coupling of the non-paretic arm, consisted of comparing EMG-triggered electrical stimulation on the paretic side wrist and nger extension both with and without wrist and nger extension executed simultaneously in the non-paretic side (Cauraugh and Kim, 2002). After 6 h of training over 2 weeks, patients with chronic hemiparesis in the coupled bilateral training group showed signicant gains in a functional task (moving blocks) as well as decreased impairments (measured by reaction times and sustained muscle contractions) compared to the unilateral training group. Moreover, the latter group showed an improvement over an attentional control group, which further demonstrates the efcacy of bilateral coupling over and above the already benecial electrical stimulation protocol. However, there was no attempt to measure further up the model of rehabilitation. Taken together, these three studies imply that bilateral training should, at a minimum, be considered as part of rehabilitation in patients with unilateral (as well as bilateral) upper extremity dysfunction. It is important to add that encouraging bilateral actions in such patients has an additional advantage other than the suggested neuromotor coupling facilitation. This advantage involves the non-paretic arm.
Precisely because of the bilateral neural coupling mechanisms, it is likely that the so-called uninvolved side is, in fact, slightly impaired. For example, comparisons between the uninvolved arms of patients with stroke and age-matched non-disabled controls nd signicant differences in gross manual dexterity motor coordination (Desrosiers, Bourbonnais, Bravo et al., 1996), handwriting (Brodal, 1973), ngertapping speed and grip strength (Prigitano and Wong, 1997) and goal-directed aiming (Fisher, Winstein and Velicki, 2000; Velicki, Winstein and Pohl, 2000; Winstein and Pohl, 1995). Therefore, training both arms may result in benets to each although those in the non-paretic arm are likely to be few and subtle (e.g., Whitall, McCombe-Waller, Silver and Macko, 2000). The ndings of Mudie and Matyas (2000) suggest that practicing bilateral dissimilar actions is not particularly advantageous when measuring unilateral gain. However, since dissimilar but complementary roles are also tightly coupled (e.g., Perrig et al., 1999), it is very plausible that, had Mudie and Matyas measured a form of bilateral dissimilar performance as their outcome measure, they would have found a benet from bilateral dissimilar practice. As noted earlier, disabilities other than stroke may benet from bilateral practice and a strong case can be made for including bilateral tasks in rehabilitating patients with Parkinsons (and perhaps Huntingtons) disease since this may be the best route for them to offset the progressive nature of this disease. Principle 2: In continuously repetitive tasks, the arms entrain to only two stable coordination states, moving together (mirror symmetric or in-phase) and moving in opposition (anti-phase) The coupling of the limbs demonstrated in discrete aiming movements is, perhaps, even more evident when the arms are called upon to repeat movements in a continuous manner (Fig. 7). They are able to do this in a relatively effortless and controlled (stable) manner only by acting at the same time or in opposition to each other. Unlike the discrete actions described above where the hands couple to accomplish dissimilar tasks, these actions, for example, brushing the crumbs off ones body, are typically identical across the two limbs. Nonidentical repetitive actions take additional attentional effort to
7.2
Relative Phase
3.6
180
360
Required Relative Phase

Fig. 7. Schematic representation of the tendency for bilateral movements of the ngers, hands or arms to have greater phase stability at 0/360 or 0/100% (in-phase) and at 180 or 50% (anti-phase). This is the so-called seagull effect. (Adapted from Tuller and Kelso, 1989.)
resist the tendency for the limbs to adopt or entrain to similar, and particularly, in-phase actions. Empirical evidence Experiments demonstrating this principle in upper extremity work are numerous. For example the attempt to produce different rhythms with the two hands, such as two beats with one hand and three beats with the other are simply impossible for all but highly skilled drummers (Peters, 1985). Only harmonic multiples of a frequency for one hand to the other (e.g., 2 to 1 or 3 to 1) in simultaneous or alternating beats are relatively easy. In a classic study, subjects attempted to tap the index ngers of each hand at a steady frequency (1 Hz) with zero phase difference and then at 10% differences between the hand making 10 conditions with 0.5 or 50% being in complete opposition (Yamanishi, Kawato and Suzuki, 1980). Phase differences were set by visual pacing signals that, after subjects could match, were turned off. Self-paced temporal errors and their standard deviation were far less at the 0 and 50% phasing in either unskilled or skilled pianists indicating the stability of in-phase and anti-phase conditions (see Fig. 6). These results were replicated by Tuller and Kelso (1989) using visual cues; and by Semjen and Ivry (2001) who compared both auditory and visual
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cueing, nding that the former were slightly more powerful in stabilising movements to the two modes. The tendency of the limbs to entrain together is also demonstrated if a weight is added to one limb changing the natural (eigen) frequency of that limb. Like physically coupled pendulums, if asked to swing at their preferred rate, the arms will adjust to a single frequency sometimes attracted towards a socalled dominant oscillator (magnet effect) and other times evolving to a new frequency that is not necessarily halfway between either natural frequencies (Kugler and Turvey, 1987). Again, in either case, only in-phase or anti-phase movements are possible. When one arm is differentially affected by insult or disease the natural frequency of that arm is markedly different and tends to become the dominant oscillator. For example, in patients with left hemiparesis, the affected arm acted as the dominant oscillator and entrained the right arm to oscillate at the slower frequency when in a bilateral condition (Rice and Newell, 2001). Importantly, the two primary coordination states are not necessarily equally attractive. Moving inphase is usually considered more stable than antiphase as demonstrated in nger-wagging experiments by (1) increasing frequency which induces a transition from anti-phase to in-phase but not vice versa (Kelso, 1984), (2) a quicker phase-resetting after perturbation from the in-phase condition (Kelso, Scholz and Schoner, 1986), and (3) a lower standard deviation of phase in steady state conditions for in-phase (Kelso, 1984). Although the weight of experimental evidence and practical experience suggest that in-phase is always easier, there are experimental situations where in-phase and anti-phase appear at least equally stable and/or do not demonstrate transitions (e.g., preferred speed tapping, Whitall, Forrester and Song, 1999; forearm pronation and supination, Carson, Riek, Smethurst et al., 2000). One reason why some conditions do not show the in-phase superiority is that cueing by augmented sensory information (e.g., an auditory beat) seems to strengthen in-phase but not anti-phase coupling compared to natural frequency movements (see Forrester and Whitall, 2000). This implies that without a sensory cue that simultaneously guides movement initiation and provides feedback, the in-phase coordination, at least, has less relative coupling strength.
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Development and learning The developmental ability to produce repetitive bimanual actions of the arms occurs after discrete bimanual movements with simultaneous and quite sophisticated banging movements occurring before the rst birthday (Fenson, Kagan, Kearsley and Zalazo, 1976). This suggests, not surprisingly, that repetitive bilateral movements are more difcult than discrete ones. Moreover, the characteristics of stable in-phase and slightly less stable anti-phase are not innately specied since children of around 4 years of age nd it difcult to maintain and stabilise around either coordination mode when doing bimanual circle drawing (Robertson, 2001) and also when trying to nger tap (Whitall and Forrester, 2003). In other words, children demonstrate large variability around a particular coordination phase and are easily moved from one quasi-stable state to another. Not until around 6 years do the two coordination modes become more easily demonstrated in either task. By 7 years, with auditory cueing, in-phase tapping is clearly more stable than anti-phase (Wolff, Kotwica and Obregon, 1998; Volman and Geuze, 2000). As with discrete movements, bimanual tapping does not become adult-like until around 11 years of age (Wolff et al., 1998). Learning to overcome the tendency to produce repetitive in-phase and anti-phase movements has been studied by Zanone and Kelso (1992, 1997) using nger tapping. Training subjects to produce a 90 or 45% phasing relationship between the ngers required extensive trials and auditory cueing. The newly acquired coordination mode resulted in a partially decreased stability of the previously existing in-phase and anti-phase modes and individual differences in acquisition rate tended to correlate with the strength of the original in-phase and anti-phase modes in that more tightly coupled original modes resulted in a longer and less successful learning of the new pattern. The acquisition of a 90 phasing pattern for whole-arm coordination was examined comparing younger and older adults (Wishart, Lee, Cunningham and Murdoch, 2002). Both groups eventually learned the new pattern after days of practice (younger having more success) and both groups, but particularly the older group, required augmented, concurrent visual feedback in order to gain success. Overall, these studies emphasise the difculty in ac-
quiring and maintaining multiple coordination states in bilateral repetitive movements and the importance of sensory feedback and practice for this process to occur. Neural basis In addition to the anatomical and physiological evidence for the neural basis of bimanual coordination already described in Principle 2 of the Bilateral movements section (some of which, we note, were determined only from studying repetitive bimanual movements) there are some additional ndings that appear specic to the characteristics of repetitive movements. First, there are physiological and clinical data that correspond with the distinctions between the easier in-phase vs. anti-phase coupling. For example, interhemispheric local eld potentials from certain single recording sites show transient, movement-related increases in correlation whereby in-phase movements showed stronger and more correlations than anti-phase movements (Cardoso de Oliveira, Gribova, Donchin et al., 2001). With respect to activation of the SMC and SMA, fMRI demonstrated greater activation for anti-phase coupling of bimanual hand movements at both sites (Toyokura et al., 1999). Similarly, for coupling between nger exion and auditory cues, Mayville, Bressler, Fuchs and Kelso (1999) also found greater activation of movement-related EEG power in SMC with anti-phase compared to in-phase coupling. Greater activation is expected with a more difcult task and those with extensive bimanual hand skill training (professional pianists) demonstrate far less activation in M1, SMA, pre-SMA and CMA than controls reecting greater efciency with smaller numbers of active neurons (Jancke, Shah and Peters, 2000b). Clinically, patients with basal ganglia disease have an almost impossible time with repetitive anti-phase bilateral cranking movements but they are able to accomplish in-phase movements (Johnson, Cunnington, Bradshaw et al., 1998, Johnson, Bennett, Georgiou et al., 2000). However, both types of phasing are compromised compared to non-disabled (Geuze, 2001; Van den Berg, Beek, Wagenaar and Wieringen, 2000). Second, the dissociation of the neural basis for temporal vs. spatial coordination relating to interhemispheric pathways noted in the previous section
(Principle 1) is less clear in repetitive movements. Three callosotomy patients demonstrated no spatial interference when comparing mirror-symmetric (in-phase) with asymmetric (anti-phase) continuous circle drawing tasks (Kennerley, Diedrichsen, Hazeltine et al., 2002). This nding conrmed the role of interhemispheric pathways vs. lower-level interactions for spatial coupling as demonstrated in the square-drawing task also described in the previous section (Principle 1). However, they did not conrm a subcortical role for temporal coupling since this was also disrupted in the circle-drawing task. In a second experiment using nger exionextensions in the sagittal plane these patients also showed a temporal desynchronisation when the nger movements were in a condition that was continuous vs. a condition where they had to pause between each exion cycle where temporal coupling was maintained. Taken together, these results suggest that temporal synchronisation between the hands during repetitive continuous movements (but not movements with discrete events such as nger tapping) still depend on interhemispheric transmission across the corpus callosum. This implies that repetitive bilateral training may have more benets for temporal aspects of movement than discrete bilateral training if interhemispheric facilitation occurs. Implications for rehabilitation Assessment. The importance of assessing repetitive bilateral movements in rehabilitation is not immediately obvious because most upper extremity bimanual activities of daily living are not repetitive (except for arm swing during walking) but rather intermittent and goal-directed. Nevertheless, an appreciation of the concept that stable coordination is a fundamental and desirable state would lead us to suggest that bilateral (and unilateral) movement tasks should always be assessed over a number of trials in order to ascertain whether the observed coordination is stable over trials. In general, having a patient present with a variable (unstable) coordination pattern is not necessarily undesirable because it may indicate that the patient can more easily change their present movement pattern towards one more desirable. Treatment. Given the plausible advantages of bilateral arm training, already suggested in the previous
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section, are there properties of repetitive bilateral arm movements, be they continuous or regularly interspersed with discrete events, which have further benet for patient rehabilitation? While repetition of bilateral movements may not be ecologically valid, repetition per se provides intense practice of a given task. Therefore, given that a patient has a bilateral coordination decit, practicing in a repetitive fashion is likely to mean multiple practices of the task with both hands and should be encouraged (see section Practice and active participation are fundamental to motor learning below, for the benets of practice). One study that repeatedly practiced tasks in a unilateral vs. bilaterally symmetric way was conducted on patients who had almost completely functionally recovered from their stroke (Platz et al., 2001). A kinematic motion analysis was still able to detect subtle decits of stroke patients compared to nondisabled controls in aiming movements at a target. After 5 days of repetitive training on two aiming tasks and nger tapping, patients improved statistically equally on a unilateral or bilateral (dissimilar) task regardless of whether they trained unilaterally or bilaterally (symmetrically). This suggests rst that even minor decits can be improved by structured (repetitive) training and second that any advantage from bilateral training reported in other studies (Cauraugh and Kim, 2002; Mudie and Matyas, 2000) was not present in these high functioning patients. Again, a criticism of the study is that there was no outcome task that resembled the bilateral symmetrical training and therefore it is possible that a bilateral training advantage would have been seen had these movements been tested. Nevertheless, it is likely that unilateral training that has an element of repetition might be equally or even more appropriate for highly functioning patients with stroke. In addition to repetition itself, are there other advantages of practicing mirror symmetric (in-phase) or possibly anti-phase movements? One possible advantage is that since in-phase and anti-phase are the only stable coordination patterns in a developed nondisabled nervous system, it follows that they should be easier to re-acquire in a compromised system (e.g., stroke or cerebral palsy) or to practice in a diseased system such as Parkinsons or Huntingtons. A method of stroke rehabilitation called bilateral arm training with rhythmic auditory cueing (BATRAC)
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does use the principles of in-phase and anti-phase stability as well as the principle of sensorimotor entrainment to facilitate stroke recovery (Whitall et al., 2000). BATRAC consists of patients grasping (in some cases the paretic hand is tied to) unyoked handles that move across virtually non-resistive linear tracks in a pushing and pulling motion. Five minutes of bilateral in-phase actions is followed, after rest, by 5 min of anti-phase actions and then both repeated. The actions are cued by a metronome at a preferred and constant frequency. In a single-group design, after 6 weeks training chronic stroke patients of mild and moderate stroke severity showed signicant and durable changes in impairment (Fugl-Meyer UE Test of Impairment), functional limitation (Wolf Motor Time Test) and daily use (University of Maryland Questionnaire for Stroke). Given that the subjects were all well past spontaneous recovery and not receiving other treatments these results are encouraging but with no control group hardly conclusive. It is not clear whether benets were primarily from the bilaterality of the task (supporting other work), or whether repetition either of the in-phase or antiphase practice or both had additional benets. It is also unknown how important the external cue was in forcing patients to attend to the task and receive feedback. Other studies provide some insights with regard to these features. For example, in children with spastic hemiparesis, drawing circles in a mirror symmetric coordination mode resulted in a decrease of temporal variability and increased smoothness of movement in the impaired arm compared to single-handed performance (Volman, Wijnroks and Vermeer, 2002). However, in the asymmetric or anti-phase mode there was no benet and the unimpaired arm became more spatially and temporally variable. Therefore continuous repetitive tasks are enhanced only by testing (and presumably training) in-phase movements in this particular population. External cueing of movements is a useful adjunct to goal-directed movement and it appears to aid learning of coordination patterns in non-disabled (e.g., Wishart et al., 2002). However, patients with Huntingtons disease (unlike patients with Parkinsons disease, Johnson et al., 1998) were not able to use this information to perform a bilateral anti-phase cranking action (Johnson et al., 2000). Thus, external cues will not always provide
a benet but will probably be worth trying in many cases as we also suggest in the Reach and grasp section (Principle 2) above and in section How are reach-to-grasp actions learned (re-learned)? below. Principle 3: Each hand is specialised for different functions within non-symmetrical bimanual tasks Despite the strong tendency to spatially and temporally couple the limbs together in discrete and repetitive tasks, the limbs are not equal in their ease of accomplishing a specic task in a bimanual situation. Typically, where different tasks are required of the two hands, the dominant hand in a unimanual situation becomes the manipulative hand that is required to do more precise actions and the non-dominant hand becomes the supporting and stabilising hand. Thus the dominant hand will hold the spoon for stirring or pick up the tea cup, carry it to the mouth and tip to the appropriate angle while the nondominant hand will hold the saucer steady. Empirical evidence Observations of naturally occurring tasks shows that asymmetries in bimanual coordination are ubiquitous (see Peters, 1994, for discussion). The dominant hand tends to directly realise the goal of a task with precise timing relative to the preparatory and support role of the nondominant hand. In general, the dominant hand performs movements with a more continuous, precise adjustment of speed and force while the non dominant hand moves more intermittently. These characteristics are also accompanied by more continuous and focused attention to the dominant hand (Peters, 1990). In experimental situations such as the task described in the Bilateral movements section, Principle 1, where one arm moves unidirectionally and the other does a reversal, performance was worse when the left arm performs the more demanding reversal movement and the right arm the easy movement than vice versa (in right handers) (Walter and Swinnen, 1990b). Similarly, in repetitive tapping tasks (for right handers), bilateral performance is better when the right hand does the activity demanding more attention (e.g., fast tapping vs. steady beat) (Peters, 1981). In this case, the right handers also performed the less demanding task better with the left hand
demonstrating further the asymmetry in task specialisation. However, left handers do not provide the opposite scenario. Those left handers who perform both ne (i.e., writing) and gross motor (e.g., throwing and batting) tasks with the left hand tend to show no asymmetries while those left handers who only perform ne motor skills with the left hand tend to perform with the same asymmetries as right handers even though the experimental tasks (nger tapping) are ne motor (Peters and Servos, 1989). These studies not only demonstrate task specialisation but highlight the complexity of handedness in the bilateral situation. In addition to everyday or experimental tasks where hand function is differentially allocated, there are also many but subtle asymmetries seen in experiments where the actions are basically symmetrical and strong temporalspatial coupling effects were emphasised in the earlier sections. For examples of these asymmetries, see Marteniuk, MacKenzie and Baba (1984) and Sherwood (1994) for discrete tasks and Byblow, Bysouth-Young, Summers and Carson (1998) and Treffner and Turvey (1995) for rhythmic tasks. In general, these asymmetries correspond to handedness with the dominant hand leading. However, in some cases, it is the easier task that results in a leading hand (Marteniuk et al., 1984) and the size of the asynchrony itself can be manipulated by attentional cueing so that, for example, focusing on the dominant hand increases the lead in bimanual circle drawing while focusing on the nondominant hand decreases the lead (Swinnen, Jardin and Meulenbroek, 1996). Using the same task, Byblow, Lewis, Stinear et al. (2000) used a visual cue to change direction in one hand. Disruptions of the other hand occurred more often when the dominant hand changed direction suggesting an asymmetry in that the dominant hand is more strongly linked to the nondominant than vice versa. Development and learning Simultaneous but differentiated activation of the two hands cooperatively (e.g., grasping while pulling) emerges between 8 months and 1 year (Fagard, 1994). By 3 to 4 years of age, children typically show differential hand preference and skill similar to adults and by 5 years of age this is generally accepted to be stable (Tan, 1985). Between 80 and
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90% of the population establish right handedness with the rest either strongly left or mixed dominance (McManus, Sik, Cole et al., 1988; Porac, Coren and Duncan, 1980). Whether handedness is primarily driven by nature or nurture is a highly debatable and controversial topic that would have implications for rehabilitation. To our knowledge there is no empirical resolution of this question and most researchers in the eld assume some interaction between maturation of the nervous system and experience. We are also not aware of learning studies that measure the difculty in changing hand specialisation for either unimanual or bimanual tasks. The fact that some asymmetries are found in the neural basis of bimanual coordination would suggest that this is not as simple a task as one would think even in the nondisabled. One has only to tie shoe laces with hand roles reversed to understand how specialised our hands become and how much effort the process of reversing roles might take for some bimanual tasks! Neural basis We have already noted that the left hemisphere appears to show some overall control of aspects of bimanual behaviour whereas the right hemisphere does not, at least in right-handers. Other asymmetries are seen in SMA activation detected by fMRI of bimanual nger tapping in right handers (Jancke et al., 2000a). In the task where the right hand is tapping at a faster rate than the left hand, the left SMA showed more activation than the right SMA. However, during the left fastright slow task, the right SMA was not signicantly more activated than the left SMA. In contrast, activation levels in the primary SMC were not asymmetric and the SMC contralateral to whichever hand was tapping faster had the stronger activation level. Asymmetries in the functioning of corticospinal pathways have been detected using transcranial magnetic stimulation. For example, the dominant hemisphere appears to have increased excitability of cortical inhibitory processes (Matsunaga, Uozumi, Tsuji and Murai, 1998; Priori et al., 1999) and greater corticomotor representations of the hands (Triggs, Subramanium and Rossi, 1999; Volkmann, Schnitzler, Witte and Freund, 1998). In general, these results tend to be similar for both right and left handers unlike some of the behavioural data mentioned above.
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Implications for rehabilitation Assessment. From the above discussion there are two main factors to consider regarding hand specialisation: handedness of the patient and the related consequences of hemispheric asymmetry. Regarding handedness, there is little doubt that a therapist would soon determine the handedness of a patient but surprisingly this factor is not always considered in standardised arm assessment tools. For example, asking a stroke patient whether they had difculty over the last two weeks in using their paretic hand to turn a door knob or open a can or jar (Stroke Impact Scale #5) does not recognise the fact that this action would rarely be accomplished by a non-dominant hand in the non-disabled. Therefore, the score for these items is likely to be biased since a patient with nondominant paresis will not be able to accurately estimate the difculty of a task that they have not tried. The same argument holds for bimanual tasks if there is no differentiation between the roles of a dominant and nondominant arm. Unfortunately, as noted earlier, bimanual tasks are rarely assessed in formal assessment scales. One scale that takes both bimanual tasks and prior handedness into account is the recently developed University of Maryland Arm Questionnaire for Stroke (UMAQS; Whitall et al., 2000). In this questionnaire if the paretic arm is non-motor dominant, the questions relate to support rather than primary manipulative functions and vice versa. Regarding the hemispheric asymmetries and particularly the fact that the left hemisphere is important for bimanual activities means that neurological insult to one side vs. the other should manifest itself in different behavioural consequences. For example, in patients with mild subacute stroke, Giuliani, Purser, Light and Genova (1997) found that those with a left-sided lesion showed decits with both arms in nger-tapping frequency while those with right-sided lesions demonstrated loss only in the paretic arm. In a ner-grained analysis of the noninvolved arm function for reaching tasks, Winstein and Pohl (1995) found that both left and rightsided chronic stroke patients were slower compared to age-matched controls but the locus of slowing differed based on the side of stroke. Patients with left lesions had decits in the initial (feedforward) component of the reach while patients with right
lesions had difculty with the homing (feedback) component of the reach. Taken together, these studies demonstrate that side of lesion can differentially impact decits in both paretic and non-paretic arms. Treatment. How might these factors affect treatment protocols? First, therapists should realise that the functional goals for retraining handarm function from either neurological insult or injury will differ depending on the motor dominance of the affected limb. The functional goals should reect the functional roles of each handarm whether in unimanual or bimanual tasks and this concept ts well with the task-specic motor learning principle (see section below Designing practice for motor learning3). The attentional focus of a patient is also important and, particularly in diseases where there is bilateral decit (e.g., Parkinsons), a therapist should be aware that manipulating the hand focus in a bimanual task will have an affect on performance. Regarding treatment composition, however, none of the previously mentioned experimental bilateral training protocols have considered using functionally dissimilar role specialisation because they are based on the premise of facilitation of neural coupling by bilaterally symmetric actions. From the perspective of hemispheric asymmetry, we can, however, ask whether a given treatment is equally effective depending on the side of lesion. For example, given that patients with left hemisphere lesions might be expected to have a greater bimanual decit, would a bilateral training paradigm produce a response advantage or disadvantage? In 16 right-handed patients with chronic stroke, after BATRAC training, the 8 with left lesions showed a response advantage in strength measures of the non-paretic arm and in the time taken to complete functional tasks with the paretic arm (McCombeWaller and Whitall, 2002). This response advantage could relate to a bigger initial decit with more capacity for recovery but baseline differences between the groups were not found. The lack of baseline differences is in contradiction to other studies, a fact that could be explained by different measures, stroke severity and/or chronicity between the studies. A neurally based explanation of the response advantage may relate to the differential interhemi-
spheric inhibitory circuits since, as suggested earlier (see above, Bilateral movements section, Principle 1) bilateral training may disinhibit transcallosal projections. In individuals without disability, motor overow is greater from the use of the dominant arm (Armatas, Summers and Bradshaw, 1994; Todor and Lazarus, 1986) suggesting a greater inhibition of motor nondominant cortex by motor dominant cortex (in line with the Byblow et al. (2000) ndings mentioned in the previous section). Therefore, damage to the motor dominant hemisphere may show increased responsivity to disinhibition since there is increased inhibitory control prior to stroke (Whitall and McCombe-Waller, 2001). Other explanations of this nding may relate to an increased effort on the part of the subject to recover motor dominant hand function or the effects of perceptual and/or visual decits from right hemisphere damage that affect bilateral training (McCombe-Waller and Whitall, 2002). Regardless of the causeeffect, these asymmetrical ndings indicate that bilateral training may be more benecial to those patients who have lesions in the motor dominant hemisphere, at least for right handers. Bimanual movement summary We have now presented three motor control principles specically relevant for bimanual movements. Under the rst principle, we described how simultaneous bilateral movements are tightly coupled in spatialtemporal (and force) parameters for discrete movements. This coupling occurs both for similar and dissimilar handarm functions. For the second principle we extended the bimanual case to repetitive movements and noted that only two coordination states, in-phase and anti-phase, were stable with the former being usually the preferred mode. In the repetitive case, we note that the tendency for entrainment between the hands with or without sensory cueing is hard to overcome when dissimilar handarm functions are desired. Under the third principle, we considered the evidence that despite the tendency for coupling and entrainment there is still hand specialisation in the functioning of either hand in bimanual movements.
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Common ground and implications for rehabilitation Common to the previous sections are factors surrounding learning and memory. It seems obvious to us that any discussion of rehabilitation for motor control would necessarily be informed through a basic understanding of the behavioural and neurobiological mechanisms of human learning and memory. However, this practical and natural foundation has not until recently been explored to guide rehabilitation approaches (Fuhrer and Keith, 1998). In this nal section, we develop and discuss three common elements of learning in general and motor skill learning in particular, that emerged from the previous sections on Reach and grasp and Bilateral movements pertinent to the rehabilitation of upper limb movements after brain injury. The rst element is simple and based on the notion that practice is considered the most powerful variable for skill acquisition (Newell and Rosenbloom, 1981). If the goal of rehabilitation within the Top-Down model is to recover the ability to perform specic skills, then an understanding of the role that practice plays in this process is essential. The nature (passive vs. active), intensity (doseresponse), duration, timing (early, late), and conditions of that practice (task-specic, guidance, etc.) have only just begun to be explored systematically for rehabilitation (see Ezehiel, Lehto, Marley et al., 2000, Lehto, Marley, Ezekiel et al., 2001, and the four-part series ?#12 by Wishart, Lee, Ezekiel et al., 2000). For the most part, therapists use of learning principles is intuitive and the result of their own clinical experience rather than the evidence (Fuhrer and Keith, 1998; section Current clinical practice: translation from theory? above). In some cases, the evidence runs counter to practical intuitive approaches and that is when critical reminders, such as the performancelearning distinction, are necessary considerations (Cahill, McGaugh and Weinberger, 2001). The second element concerns how reach-tograsp actions are learned or re-learned through practice. We suggest that the essential control strategies are not necessarily accessible to conscious recollection and are therefore implicit in nature, but that they develop through repetition and practice. These control strategies have been characterised as perceptual
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motor linkages and/or dynamic transformations. For the most part, we describe these principles of control for reaching, grasping and object manipulation throughout the above sections Reach and grasp and Bilateral movements, but highlight the ideas of central vs. peripheral contributions as they pertain to practice and skill learning. Finally, the third element of learning discusses how to design the practice session for effective learning. We describe the neural correlate of the performancelearning distinction and reect back on the Thorndike (1927) Law of Effect by emphasising the importance of meaning and motivation to learning. In this case, we suggest that the nervous system must recognise the task for it to be meaningful as a tool in rehabilitation. This notion of learning for rehabilitation of reaching and grasping actions can explain in part the effectiveness of rehabilitation programs that emphasise real-world task practice (i.e., task-specic approach) over those that emphasise impairment-level practice such as musclespecic resistance, endurance training or spasticity reduction. Further, as discussed in the above section Reach and grasp, Principle 2, the neural substrate for grasping actions provides a kind of functional vocabulary for skill learning. Practice and active participation are fundamental to motor learning A major paradigm shift in rehabilitation medicine has come about primarily due to the recognition and application of the principles associated with the acquisition of motor skills to treatments aimed at the recovery and rehabilitation of movement following disease or injury. This quiet revolution has evolved slowly as the traditional views in neurobiology of relatively permanent and xed impairments have given way to more recent views that embrace the plasticity of the brain and spinal cord systems through activity-dependent, use-dependent, and learning-dependent processes (Johansson, 2000; Nudo et al., 1996; Plautz, Milliken and Nudo, 2000; Tillerson, Cohen, Philhower et al., 2001). While an awareness of therapy-triggered adaptation in the damaged nervous system is not new, its acceptance has only recently been embraced by the rehabilitation community to the point of becoming an ex-
pected outcome. Indeed, a 1915 preliminary report written by the well known physician-scientist, Shepherd Franz and colleagues titled: The possibility of recovery in long-standing hemiplegia was virtually ignored until recently, perhaps as a consequence of the mostly incongruent and relatively stagnant view of the brain that dominated medical practice nearly a century ago (Franz, Scheetz and Wilson, 1915). The motor learning effect provides a viable explanation for the benets of practice in physical rehabilitation especially after the transient and early physiological effects of spontaneous recovery have passed. For behaviour, motor learning is dened as a set of processes associated with practice leading to a relatively permanent change in the capability for responding (Schmidt and Lee, 1999). In other words, and for any therapeutic intervention that promotes task practice, one can argue that task practice itself is designed to lead to benecial changes in multi-joint performance through control capabilities that are retained and transferred to real world activities such as reaching and grasping actions. The most fundamental law of motor learning is practice and therefore, rehabilitation programs that promote higher doses of practice have been generally successful (Keith, 1997; Kwakkel, Wagennar, Koelman et al., 1997; Van der Lee, Snels, Beckerman et al., 2001). Active participation is important for motor skill learning The promotion of voluntary use of the centrally paretic upper limb is the only common parameter across a varied set of investigations that have resulted in improved function and not simply a reduction in impairment (Butesch et al., 1995; Cauraugh et al., 2001; Dean and Shepherd, 1997; Kraft, Fitts and Hammond, 1992; Kunkel, Kopp, Muller et al., 1999; Lum et al., 2002; Sunderland, Tinson, Bradley et al., 1992; Taub, Miller, Novack et al., 1993; Tangeman, Banaitis and Williams, 1990; van der Lee et al., 1999; Whitall et al., 2000; Wolf, Lecraw, Barton and Jann, 1989). How the use of the centrally paretic limb was promoted varied considerably across these studies from electromyography-triggered neuromuscular electrical stimulation (Cauraugh et al., 2001) to repetitive force production against resistance (Butesch et al., 1995). More clinical research is needed to determine if there are any differences in out-
comes from these various approaches (e.g., forceduse, EMG-triggered ES, resistance strength training; bilateral arm training) or if a combination of the specic practice protocols are best (e.g., forced-use and EMG-triggered ES). Equally important to the dose of practice is the need for active participation regardless of how the practice and use is promoted. For example, in the case of electromyography-triggered neuromuscular electrical stimulation, it is active wrist extension that triggers the electrical stimulation for assisted wrist extension. The training program is designed to gradually progress (challenge) the amount of active wrist extension (i.e., demanding more active motion) over time that is needed to trigger the electrical stimulation. Active participation is fundamental to skill acquisition. This requirement may explain in part why there are no clear answers from comparative studies of different physical therapy approaches with a heterogeneous group of patients each with a custom designed therapy program (Wagenaar, Meijer, van Wieringen et al., 1990). Well-designed randomised controlled trials of specic components of therapy delivered in a systematic and quantiable dose such as neuromuscular electrical stimulation (Glanz, Klawansky, Stason et al., 1996), 10 h of additional NDT to the upper extremity (Parry, Lincoln and Vass, 1999), 2 weeks of forced-use (van der Lee et al., 1999), or even 20 h of additional functional training to the upper extremity in the 46-week acute phase after stroke (Winstein, Rose, Chui et al., 2001) have all led to functional gains in performance, but only in less severely impaired patients who have some residual capability for voluntary movement. The initial level of impairment is therefore an important moderating variable underlying the therapeutic effectiveness literature. Results such as these suggest that upper extremity training programs for subjects with central paresis should be aimed at those with at least a minimal level of voluntary control of the arm and hand a level that is compatible with active participation. Specic criteria for that minimal level vary across studies. For example, the primary criteria for patient eligibility for a forced-use (also known as constraint-induced therapy (CIT)) intervention includes, the ability to initiate at least 20 degrees of wrist extension and at least 10 degrees of extension at two digits and the thumb of the
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affected hand, in addition to adequate balance and safety while wearing the restraint. These criteria are derived from electromyographic (EMG) biofeedback studies (Wolf and Binder-Macleod, 1983) that indicated voluntary movements of nger and wrist extension were a better predictor of future acquisition of independent limb use than was the ability to reduce the hyperactive responses from stretching upper extremity exor muscle groups (impairmentlevel). The number of patients that actually achieve this level of functional recovery in the upper limb after a stroke is estimated to be approximately 20 25% of the population (Wolf, Blanton, Baer et al., 2002). With respect to voluntary use, these criteria are important indicators of potential reacquisition of meaningful function. Since the majority of upper extremity use involves reaching, grasping and manipulating objects, the anticipatory and preparatory movements of wrist and nger extension of the centrally paretic limb and the capability to modulate force are essential to achieving at least some task success for functional activities without requiring outside assistance (either from the other limb or another person). Attempts to quantify the residual hand function that is associated with optimal recovery suggests 80 90% preservation of the corticospinal (pyramidal) tract and minimal Wallarian degeneration (Feydy, Carlier, Roby-Brami et al., 2002; Seitz, 1997). The importance of severity of arm impairment for responsiveness to therapy is emphasised in the recent literature and Canadian clinical consensus panel (Consensus Panel, 2001; Parry et al., 1999; Partridge, Mackenzie, Edwards et al., 2000; Shelton, Volpe and Reding, 2001) but has not been used systematically to guide rehabilitation practice (De Weerdt and Feys, 2002; see above section Current clinical practice: translation from theory?). Motor learning is not just the establishment of stimulusresponse connections formed by reward or destroyed by punishment A motor learning perspective provides a viable interpretation of the critical elements underlying these specially focused rehabilitation approaches such as forced use after stroke (Morris, Crago, DeLuca et al., 1997). The family of therapies referred to as CIT consists of at least two important elements. One is
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the restraint of the less impaired limb. The other is intense and extensive training or practice of functional activities with the more impaired limb for a period of at least 6 h/day over a 2-week interval (Taub and Wolf, 1997; Taub et al., 1993). Previous research has suggested that the effectiveness of CIT is enhanced through the combined effects of restraint and practice (Taub et al., 1993) compared to a condition with restraint alone (Wolf et al., 1989). It has been suggested that the practice element accounts for approximately 80% of the benet, while the restraint accounts for the other 20%. In spite of the obvious benets from constraint-induced practice, the primary hypothesis proposed to explain the effectiveness of CIT is the reversal of learned non-use. The concept of learned non-use was rst introduced by Janet Tries, an occupational therapist, in connection with incontinence rehabilitation (Tries, 1991). Taub and colleagues have extended and elaborated the hypothesis and propose a rather simplistic, stimulusresponse behavioural explanation (i.e., operant conditioning) which posits that early attempts to move the paretic limb are unsuccessful; this reinforces non-use (i.e., conditioned suppression), and eventually the patient has learned to avoid task solutions which involve any use at all of the centrally paretic limb (Taub, Crago, Burgio et al., 1994). Indeed, Taub has suggested that the primary mechanism underlying the effectiveness of CIT is the lifting of conditioned suppression of latent behaviours (Morris et al., 1997; Taub et al., 1994). In a recent critical analysis of the existing CIT studies, Wolf and colleagues summarise the support for the two primary mechanisms proposed for the effects observed after CI therapy overcoming learned nonuse, or use-dependent cortical reorganisation. To date, the evidence is far stronger for the latter than the former (Wolf et al., 2002), but see Sterr, Freivogel and Schmolohr (2002) for recent evidence of neurobehavioural discrepancies between residual movement capabilities and spontaneous use in support of learned nonuse. While it is tempting to accept an operant-conditioning explanation for CIT, Cahill and colleagues remind us that simplicity is seductive and often wrong (Cahill et al., 2001, p. 580). The simplistic and inuential ideas of the early 1900s suggesting that all animal behaviour could be explained through
stimulusresponse connections formed by rewards or destroyed by punishment have, for the most part, been rejected in the face of more contemporary experimental evidence. Even Sir Charles Sherrington in his classic work, The Integrative Action of the Nervous System (Sherrington, 1911), remarked that the simple reex arc was more a convenient ction. Indeed, recent work concerning proprioceptive reexes has revealed considerable contextand phase-dependent properties and learning-related phenomenon (Hodgson et al., 1994; Stewart, 2002; Wolpaw and Tennissen, 2001) that cannot be explained by a simple stimulusresponse connection. We now understand that motor learning of voluntary skills is a highly complex problem-solving process that cannot be explained by specic responses made to specic stimuli (Lee, Swinnen and Serrien, 1994), nor to information processing of any discrete neural region (e.g., primary motor cortex). Further, we cannot reject the idea that more of the same is possibly the basis of improvements seen with CIT (van der Lee, 2001). Taken together, the neurobiology of motor skill learning likely involves a distributed network with parallel and serial processing of functionally dissociable explicit and implicit memory and learning systems. How are reach-to-grasp actions learned (re-learned)? Consideration of implicit and explicit processes: procedural and declarative memory and learning systems The broad construct of memory can be subdivided into at least two main types declarative and procedural which differ fundamentally in the kind of knowledge each stores and processes (Squire, 1987). Declarative (explicit) memory deals with knowledge of facts, events, and episodes. It may be formed very quickly (even in one exposure) and is directly accessible to conscious recollection (Squire, 1987). Procedural (implicit) memory is the capacity to acquire perceptualmotor skills (knowledge) through physical practice and is not directly accessible to conscious recollection as facts or data. A good example of this is learning to ride a bicycle (Polanyi, 1958). Most physicists know the rule (explicit knowledge): turn the handlebars so that the
curvature of the bikes trajectory is proportional to the angle of its imbalance, divided by the square of its speed. Most experienced bicyclists do not know this rule stated as such; however, at some level, this knowledge summarised in the rule is embodied in the neural networks that allow cyclists to stay erect while cycling. The rule is known implicitly and is expressed by the skilled performance. The development of procedural knowledge occurs incrementally with practice, over a period of time and exposures (Brooks, Hilperath, Brooks et al., 1995; Segar, 1994). Procedural memory is likely implemented by a distributed neural network including the sensorimotor cortical areas, basal ganglia, and cerebellum. It is unclear whether during unilateral movements this network is lateralised to the contralateral hemisphere, but some evidence suggests that it is not (Boyd and Winstein, 2001; Hazeltine, 2001). Strong evidence for the dissociation of declarative and procedural memory comes from the nding that individuals with medial temporal lobe damage suffer profound declarative decits while retaining procedural memory capabilities (Nissan and Bullemer, 1987; Reber and Squire, 1998). Robust implicit learning in individuals without brain pathology has been demonstrated using different paradigms (Knowlton, Mangles and Squire, 1996; Knowlton and Squire, 1995). In one, the serial reaction time (SRT) task, subjects are cued repeatedly to respond as fast as possible to a set of different coloured lights when lit by pushing a corresponding button (Nissan and Bullemer, 1987). Unknown to the participant, she/he can be cued by a repeating sequence of stimuli (e.g., red, blue, yellow. . . etc.). With practice, participants reaction times during the sequence become increasingly faster compared to that during a random sequence of stimuli. Nissan and Bullemer (1987) demonstrated that healthy individuals were able to signicantly decrease reaction time (RT) over practice (80 trials of responses). Healthy individuals often gain explicit awareness of the sequence in the latter phases of practice, but exact recall is rare. Some evidence suggests that implicit motorsequence learning is impaired after stroke-related unilateral sensorimotor area brain damage (Boyd and Winstein, 2001) and other evidence suggests that it is spared (Pohl, McDowd, Fillion et al., 2001). Dis119
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crepancies in these ndings most likely stem from differences in task complexityintrinsic cues, stroke severity, and lesion location. It has been shown that following unilateral stroke individuals retain the ability to learn new motor skills (Hanlon, 1996; Platz, Denzler, Kaden and Mauritz, 1994; Winstein, Merians and Sullivan, 1999). However, in most motor learning investigations, participants have conscious, explicit awareness and feedback (knowledge of results) about task goals and requirements during practice. This increases the likelihood that the declarative memory system is invoked to augment implicit motor learning (Boyd and Winstein, 2001). Previous work has shown that extended and focused practice can promote explicit memory function in individuals with profound declarative memory loss (Butters, Glisky and Schacter, 1993; Glisky and Schacter, 1987, 1989). Surprisingly, there is almost no research pertaining to the impact of explicit knowledge on forms of implicit motor learning. There has been some interesting research dealing with the focus of attention (interval vs. external) for motor learning showing that an external focus of attention is more benecial for motor learning of complex balance than an internal focus of attention (Shea, Wulf, Whitacre and Park, 2001; Wulf, Shea and Park, 2001; Wulf and Weigelt, 1997). In addition, there has been some recent work pertaining to the locus of automaticity. Lang and Bastian (2002) examined whether cerebellar damage disrupts the ability to make a practiced movement more automatic. They used a dual task paradigm with tasks that did not have overlapping sensory or motor requirements for execution. The motor task required subjects to maintain an upright posture while performing a gure-8 movement using their arm. The secondary task was an auditory vigilance task where subjects listened to letter sequences and were asked to identify the number of times a target letter was heard. Cerebellar subjects were able to improve movement to a limited extent with practice. Unlike controls, the motor performance of cerebellar subjects deteriorated to pre-practice levels when attention was focused away from the movement during dual task trials. Control subjects insensitivity to dual task interference after practice was due to learned movement automaticity and was not a reection of better dual task performance generally. These ndings sug120
gest that the cerebellum may be important for shifting performance from an attentionally demanding, unpracticed state to a more automatic practiced state. Further research and understanding in this area will undoubtedly have important implications for motor skill rehabilitation. Almost no work has explored the potential to exploit what Crick and Koch (1998) refer to as zombie systems a system responsible for automatic behaviours that does not depend on conscious thought or perception for rehabilitation. It is possible that future explorations of this kind might prove particularly useful for designing rehabilitation programs. Perceptionaction linkages are formed with motor learning Evidence from more recent research concerned with the control of visually guided reaching behaviour suggests that there are at least three serially organised stages of processing. The rst is concerned with visuomotor transformations, where visual information about target position is translated into an internal reference frame, and information about object affordance is translated (see below section Designing practice for motor learning). The second stage involves trajectory specication, where a time series of body positions is specied and the kinematics of the movement are developed and stored. The third stage involves dynamic transformations, where the specied trajectory is transformed into dynamic properties reecting the torques required to complete the motion. The effects of practice and experience can be reected across each of these stages. Some investigators have suggested that the skill learning process proceeds serially through these stages with higher levels of skill characterised by an efciency of kinematic and then kinetic transformations (Marteniuk and Romanow, 1983; Sainburg, 2002; Shadmehr and Mussa-Invaldi, 1994). From a neuromotor control perspective, psychophysical studies reveal that voluntary reaching and grasping movements are governed by certain laws or principles described earlier and which can be modied through practice and learning (Ghez and Krakauer, 2000). One of the most pervasive psychophysical laws of motor control is that for aiming movements there is a trade-off between speed of movement and its accuracy (Fitts, 1954; Winstein,
Grafton and Pohl, 1997). This powerful law breaks down in the case of bilateral movement control and gives way to a coordinative structure governed by the emergence of temporal synergy. In addition and related to Fitts Law, fast movements are less accurate and more variable than slow ones (Schmidt, Zelaznik, Hawkins et al., 1979) and even faster movements made without visual feedback are also more variable in both extent and speed. One factor that contributes to this increase in variability is recruitment of additional motor units to produce rapid increases in force. It is well known that the excitability of motor neurons is subject to random variations. As force increases, uctuations in the number of motor neurons leads to proportionately greater uctuations in force and the velocity, at least up to approximately 70% of maximum voluntary force (Sherwood and Schmidt, 1980). In addition and more importantly for patients with movement disorders, movement variability may also arise because subjects may be uncertain about the forces and loads that are needed to oppose movements (i.e., the dynamic transformations). This uncertainty is known to decrease with practice, so that both accuracy and speed increase with practice (Georgopoulos, Kalaska and Massey, 1981; Newell and Rosenbloom, 1981). The ability to utilise prior knowledge of, or experience with, a predictable stimulus to modify both automatic and voluntary responses has been referred to as a central-set effect (Evarts, Shinoda and Wise, 1984). With practice and experience, central set enables descending commands to preset aspects of a response in advance of a stimulus and to anticipate the necessary forces and loads to control the movements (Flanagan and Wing, 1997; Johansson and Cole, 1994; Winstein, Horak and Fisher, 2000). It is well known that goal-directed movement paths to targets become straighter and less variable with practice and experience (Georgopoulos et al., 1981; Darling and Cooke, 1987). Such changes with practice and experience suggests a progressive use of feedforward over feedback mechanisms as well as the renement of internal forward models (Blakemore, Wolpert and Frith, 2000; Gordon, Ghilardi and Ghez, 1995; Kawato and Wolpert, 1998; Tong et al., 2002). In Principle 3 of the Bilateral movements section, we described how each hand was specialised within nonsymmetrical bilateral tasks. Sainburgs
dynamic dominance hypothesis is based on inverse dynamic analysis of dominant and non-dominant aiming movements (for sake of this argument, we assume the dominant side has had more practice and experience). He demonstrated that dominant arm movements were produced with a fraction of the mean squared muscle torque computed for nondominant arm movements made at similar speeds. As such, these interlimb asymmetries in control are thought to arise downstream to visuomotor transformations, when dynamic variables that correspond to the forces required for motion are specied (Sainburg, 2002). Sainburgs work provides a good example of how the study of natural asymmetries (related to a different use history and skill level), can be used to inform the motor skill acquisition process. Central vs. peripheral changes with learning Part of the rehabilitation of motor control of upper limb skilled actions necessarily involves an understanding of how to enhance voluntary muscle activation in cases of central paresis. The use-dependent changes with practice described earlier have been variously attributed to central control mechanisms such as changes in the cortical networks representing the action and also referred to as the neural training hypothesis reecting the voluntary drive to the muscle(s). Alternatively, and depending on the intensity, focus, and duration of the training, others have attributed these changes, particularly changes in strength (torque generating capability) to peripheral mechanisms such as the intrinsic force-generating capability of the muscle itself and also referred to as the muscle adaptation hypothesis. The common argument has been that if there is a signicant increase in strength following a short-duration isometric training bout, it is unlikely that the strength gain can be attributed to any real change in the muscles intrinsic force-generating capacity (Enoka and Fuglevand, 1993; Sale, 1988). Previous research showed that imagined training of the adductor digiti minimi muscle increased voluntary strength in that muscle as much as actual training in healthy subjects (Yue and Cole, 1992). These data strongly support the neural training hypothesis of strength training. However, a recent study failed to replicate the imagined training effect and the neural training hypothesis by measuring volun121
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tary activation with twitch interpolation before and after training (Herbert, Dean, and Gandevia, 1998). The two studies differed in that different muscles were used (elbow exors vs. adductors of the mini digit), fewer and shorter training contractions for the more recent study (Herbert et al., 1998), and a longer training period for the recent study (8 vs. 4 weeks). The only factor that might explain the differing ndings relates to the muscle being trained. Previous work suggests that there may have been more potential for increasing voluntary activation in the intrinsic nger adductors than in the elbow exors. The possibility exists that imagined training may be more effective for those muscles with rather lower initial levels of voluntary activation; something that applies here for healthy subjects, and maybe even more so to those with central paresis. Although not a classic isometric resistance training protocol, Page and colleagues found some benet from a 6-week program of combined therapy plus imagery (mental practice) for the paretic upper limb compared to a therapy only group of patients who were between four weeks and one year post stroke (Page, Levine, Sisto and Johnston, 2001). This is, however, a relatively unexplored area of research. Several recent studies have identied the same neural activation pattern for imagined and actual movements (Laeur, Jackson, Malouin et al., 2002) suggesting that motor imagery using repeated mental practice might be an effective form of practice (Jackson, Laeur, Malouin et al., 2001). However, the benet resulting from actual motor training has been shown to be superior to training using mental practice alone in healthy subjects (Hird, Landers, Thomas and Horan, 1991; Pascual-Leone, Grafman and Hallett, 1994). The effects of mental practice seem to be temporary and only when combined with longer-term actual motor practice does it benet performance and learning in healthy subjects. This suggests that a combined program of mental and active task practice could be an effective therapeutic strategy in patients with central paresis (Page et al., 2001). In summary, the acquisition of motor skill in cases of central paresis is likely mediated more by central control changes at each of the three stages of processing than by peripheral changes; however, some amount of peripheral change can be a by-product of
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repetitive practice and contribute to changes in functional performance (Butesch et al., 1995; Weiss, Suzuki, Bean and Fielding, 2000). Candidate mechanisms for these central changes include the facilitation of central set phenomenon through perception action linkages, development of effective dynamic transformations, and increased reliance on forward internal models described earlier in the Reach and grasp section above. Designing practice for motor learning In the clinical setting, it is should not be particularly surprising that motor performance improves with practice. Rather, if performance does not improve with practice, this would trigger a red ag for disease progression or its corollary. What is more important for recovery and rehabilitation is an understanding of how to design that practice so that it leads to a relatively permanent change in the capability for responding in a meaningful and functional way (the expression of skill). All too often, we forget about the seductive and often misleading temporary changes in performance and take them to reect learning when in fact, little persistence of that change is evident even after a short interval (Winstein, 1987; Winstein, Pohl, Cardinale et al., 1996). Clinical research studies that incorporate retention and transfer tests and use functional performance outcome measures (assessment tools) are sensitive to the performancelearning distinction and the utility to demonstrate motor learning. The nervous system has evolved to be exible, a necessary asset for adaptation under changing conditions. However, some degree of persistence is necessary for motor skill learning; it is that relative persistence that distinguishes a more temporary adaptive change for example, the reex gain of the vestibulo-ocular response (Rambold, Churchland, Selig et al., 2002) from a relatively permanent change in skill, for example, the acquisition of precision grip to manipulate chopsticks that evolves with practice of functional and complex skills (Wulf and Shea, 2002). While the reex adaptation model has often been used as a model for motor learning (Lisberger, 1994), we emphasise a functional distinction that is unique for the re-acquisition of motor skills involving reaching and grasping actions in rehabilitation.
Neural correlate for the performancelearning distinction The well-known performancelearning distinction has neural correlates as well. Classen, Liepert, Wise et al. (1998), using transcranial magnetic stimulation (TMS) demonstrated a form of rapid plasticity of the human cortical movement representation for thumb movements induced by practice (Classen et al., 1998). With a clever paradigm, they used focal TMS of the motor cortex to evoke directionally specic thumb movements. Participants then practiced voluntary thumb movements in the opposite direction for between 5 and 30 min. After practice, the TMS-evoked thumb movements were in or near the practiced direction and not the original pre-practice direction. This performance effect was however transient with the evoked responses eventually returning to the pre-practice direction within a few minutes. This rapid yet transient change with practice suggests a plasticity in the cortical network representing the thumb that encoded the kinematic details of the practiced movement a kind of shortterm memory representation that may reect an early stage of skill acquisition, what Karni, Meyer, ReyHipolito et al. (1998) have termed fast learning. Methods to enhance this rapid plasticity have recently been explored using the same paradigm, but with D-amphetamine (Butesch, Davis, Sawaki et al., 2002). In this case, with D-amphetamine, the voluntary motor practice resulted in an increased magnitude, faster development and longer-lasting duration of use-dependent plasticity compared to a placebo condition. These results document a facilitatory effect of D-amphetamine on use-dependent plasticity, and suggest a possible mechanism mediating the previously reported benecial effect of this drug on functional recovery after cortical lesions (Crisostomo, Duncan, Propst et al., 1988; Feeney, Gonzalez and Law, 1982). Karni et al. (1998) provided convincing evidence from MRI data that skilled motor performance is acquired in several stages. The rst stage, or fast learning is relatively transient and occurs rapidly within the rst practice session. The second stage, termed slow learning is reected by delayed, incremental gains in performance that emerged after extended practice. They suggested that this time course may reect basic mechanisms of neuronal
plasticity in the adult brain that subserve the acquisition and retention of many different skills. Other functional imaging studies using the serial reaction time paradigm have shown a shift over practice from performance of an unordered, attention demanding explicit set of components to a more automatic sequence that was accompanied by a decrease of activation in the cerebellum and prefrontal cortex (Grafton, Hazeltine and Ivry, 1995). The dynamic changes in activation over practice of various brain regions has been captured using fMRI and TMS methods where there is an increase in activation early in practice followed by a decrease as practice progresses (Pascual-Leone et al., 1994; Toni, Krams, Turner and Passingham, 1998). The relationship between these brain changes and the behavioural changes during learning are still controversial as more rened methods of experimental testing are developed (see for example Seidler, Purushotham, Kim et al., 2002). The importance of practice for motor learning cannot be underestimated in the context of rehabilitation. However, the term practice can be interpreted in many different ways. At one level, practice could involve rote repetition of movements at the impairment level of the disablement model. For example, practice might involve the repetition of a meaningless movement that requires multi-joint motions counter to a dominant synergy (e.g., simultaneous forearm supination with shoulder exion and elbow extension). Or, practice might involve purposeful repetition of the same movement. This kind of practice would involve repetition of a purposeful act such as reaching for a cup in the exact same location with the exact same movement strategy on each repetition (constant practice). Taken a step further, practice can be purposeful and repetitive, but aimed at progressive skill improvement over repetitions. In this case, there would be an explicit goal to increase efciency and effectiveness over a set of practice trials. Here, for example one subgoal might be to reduce the movement time for the task with practice without compromising accuracy. Finally, practice can also refer to a problem-solving event in which the task is constructed as a motor or environmental problem that requires the planning and execution of a movement solution (Marley, Ezekiel, Lehto et al., 2000). The design of practice as a real-world prob123
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lem in a rehabilitation setting requires a focus on the functional limitation and disability level of the disablement model and the skills and roles level of the Top-Down model. The notion that practice which is designed to challenge the problem-solving process is superior for skill learning compared to that with less or no problem-solving challenge is supported extensively in the literature for young, non-disabled individuals and more recently has been extended to the rehabilitation community (Gentile, 1998; Lee, Swanson and Hall, 1991; Swanson and Sanford, 1995; Winstein, 1991). Further, Plautz and colleagues demonstrated a corollary of this effect using a primate model in the modication of movement representations in motor cortex from repetitive practice (Plautz et al., 2000). When the monkeys practiced retrieving banana pellets from the easy, large-diameter food wells, there was no change in the areal extent of the distal forelimb movement representations in M1. However, signicant changes in the extent of the same movement representations resulted from practice when the monkey retrieved banana pellets from the more difcult, small-diameter food wells. These ndings lead to the learning-dependent hypothesis of cortical plasticity in sharp contrast to the use-dependent hypothesis. Basically, small-well retrievals became more efcient and the pellet retrieval strategy changed (e.g., more selective individual nger movements and quick nger icks to ip the pellet out). These changes reected the acquisition of a new motor skill that was indicated by the emergence of a new retrieval movement pattern in parallel with improvement in retrieval efciency (fewer nger exions for each retrieval), and the corresponding cortical representations in M1 reorganised to reect this skill acquisition. This suggests that the signicant cortical re-organisation (neuroplastic changes) induced by practice comes about not from mere repetition, but from a motivation to solve the movement problem (challenged but within reach. . . no pun intended). The nervous system must recognise the movement problem for it to be effective as a tool in rehabilitation We suggest that when practice is designed in the context of a motor or environmental problem, the damaged nervous system is more likely to recognise
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the movement problem, formulate revised or new perceptionaction linkages and respond through ecologically valid control solutions. Indirect evidence for this was (1) the mirror-neuron (dealt with in the Reach and grasp section, Principle 2), and the idea that in the primate, a subset of F5 neurons behave as an observationexecution matching system, (2) that occupationally embedded exercise programs result in better outcomes than rote exercise programs (Lin et al., 1997), and (3) that the pre-sense of a real object provides a better stimulus than an imaginary or nonexistent object during training (Wu et al., 2000). Parallel concepts have been put forward to explain the benets of locomotor re-training in spinal cord and stroke through the use of body-weight supported treadmill training (Barbeau and Fung, 2001). Several critical elements of this training that derive from the neurophysiology of locomotion are the erect trunk posture, the reciprocal patterning of the legs, and the trailing posture of the stance limb prior to the stanceswing transition all of which help the nervous system recognise the motor problem of walking. Training with a standard rolling or pick-up walker for cases of incomplete spinal cord injury or a cane for cases of stroke does not promote these critical movement elements and does not resemble walking. Indeed, for select populations, these standard methods of locomotor re-training have been shown to be less effective for recovery of locomotor skills than a program that includes body-weight supported training (Behrman and Harkema, 2000; Sullivan, Knowlton and Dobkin, 2002). Summary and conclusions In this chapter we have set out principles of motor control with application to motor rehabilitation. In a section on reach and grasp movements we covered three principles pertaining to (1) straight-line nature of hand paths, (2) separate visual pathways mediate perception and action, and (3) action involves a mix of feedback, reactive and feedforward, predictive control. In the following section on bilateral movements we noted principles: (1) under task situations requiring simultaneous movements, the arms are coupled as a unit; (2) in continuously repetitive tasks, the arms entrain to only two stable coordination states, moving together (mirror symmetric
or in-phase) and moving in opposition (anti-phase); (3) each hand is specialised for different functions within non-symmetrical bimanual tasks. Finally, we reviewed a number of points of common ground across the principles concerning learning and implications for rehabilitation. Our approach has a strong bias towards the details of movement and the underlying processes contributing to movement. As such we might be criticised for overemphasising pathology when, as we discussed in our opening section on models of impairment, the key need is for application that contributes to outcome. While acknowledging the limitations of our approach, we nonetheless remain condent that it is through careful and detailed analysis of the elements of motor control that, ultimately, will come robust and applicable understanding that will address all levels of the ?#15 disablement model. Acknowledgements ?#16 Paulette van Vliet, Ailie Turton, Helen Hill. ?#17 References
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Please see next page for author queries
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QUERIES: ?#1: Please check location of call-outs to Figs. 3 through 7; also, are these the correct gure captions? there were two versions. (page 82) ?#2: Homes or Holmes? see refs. (page 86) ?#3: is Franz VH the correct ref. here? (page 91) ?#4: Rizzolatti et al. 1997b correct? (page 92) ?#5: Rizzolatti et al. 1997a? (page 92) ?#6: Please include Flanagan, 1993, 1994 in ref. list. (page 97) ?#7: Babbe Ratin et al. (EBR): Please give ref.; EBR? (page 101) ?#8: Ramsay or Ramsey? see refs. (page 104) ?#9: Preilowski or Prelowski? see refs.; Franz EA et al. here? (page 106) ?#10: Keshevan or Keshavan? see refs. (page 106) ?#11: Armitas or Armatas? (page 115) ?#12: Ezehiel et al.: 2000 in refs. Should the remaining three parts in the Wishart et al. series be included in the ref. list? (page 116) ?#13: Segar or Seger? (page 119) ?#14: Check spelling: Nissan (Nissen) and Bullemer, 1987 (page 119) ?#15: The following references are not cited in the text: Bernstein, 1967; Eliassen, Baynes and Gazzina, 1999; Eliassen, Baynes and Gazzaniga, 2000; Flanagan and Wing, 1993; Gentilucci, Castiello and Corradini, 1991; Jeannerod, 1986; Jeannerod, 1994; Keith and Cowell, 1987; Kermadi, Liu, Tempini et al., 1998; Schmidt and Young, 1987; Viviani, Perani, Grassi et al., 1998; Flanagan, Tresilian and Wing, 1993b (page 125) ?#16: Please give details. (page 125) ?#17: The following are cited in the text but not present in the reference list: Cauraugh et al., 2001. Flanagan, 1993. Flanagan, 1994. Peters, 1985. Wolpert and Kawato, 1998. Jenmalam et al., 1998. Please supply these missing refs. (page 125) ?#18: First and last pages of chapter? (page 125) ?#19: Publisher + location? (page 125) ?#20: Vol. number? (page 126) ?#21: Is journal name correct? (page 126) ?#22: Please check journal name. (page 127) ?#23: Initials of authors and full journal name, please. (page 127) ?#24: Journal name in full, please. (page 129) ?#25: Journal name correct? (page 130) ?#26: Journal name in full, please. (page 130) ?#27: Volume number? (page 132) ?#28: Vol. and page numbers missing. (page 133) ?#29: Vol. number? (page 133) ?#30: Check journal name, please. (page 133) ?#31: Title of edited volume? (page 133) ?#32: Journal name correct? (page 133) ?#33: Journal name in full, please. (page 134) ?#34: Check journal name. (page 134) ?#35: Full name of journal correct? (page 135) ?#36: Please update; submitted where? (page 136)
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2003 Elsevier Science B.V. All rights reserved Handbook of Neuropsychology, 2nd Edition, Vol. 9 J. Grafman and I.H.

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C. Winstein, A.M. Wing and J. Whitall

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Health Condition (disorder/disease)

Contextual a. Environmental b. Personal

Ability to achieve meaningful goals with consistency, flexibility, and efficiency.

Fig. 2. Top-Down Model of Rehabilitation (Gordon, 2000).

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Elbow extensor torque

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C. Winstein, A.M. Wing and J. Whitall

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C. Winstein, A.M. Wing and J. Whitall

Forward dynamic model Forward output model

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Required Relative Phase

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