NEUROPSYCHOLOGICAL REHABILITATION, 2002, 12 (4), 289310

Cognitive rehabilitation for unilateral neglect:

Review
Tom Manly
Addenbrookes Hospital, Cambridge, UK

Unilateral spatial neglect, a striking difficulty in paying attention to one side of

space, is a common consequence of cerebro-vascular disease. Although most
patients appear to recover from this deficit relatively quickly, chronic forms
of the disorderusually resulting from right hemisphere damage and affecting
left spaceare associated with slowed motor recovery, poor response to
rehabilitation, and difficulties in many everyday activities. This article reviews
the theoretical underpinnings and efficacy of rehabilitation techniques including;
behavioural training in leftward visual scanning, eye-patching, encouraging
movement of the left limbs, and interventions designed to increase general
alertness. Recent highly positive results from brief adaptation training with prism
lenses are discussed. Neglect is a heterogeneous cluster of deficits that can
arise following damage to a variety of brain structures. It is not yet clear whether
one rehabilitation technique will be appropriate for all patients/manifestations of
the disorder, or whether combining different interventions may produce additive
benefits. There is growing evidence that chronic neglect is associated with
indeed possibly fostered bylimitations in a number of non-spatial attentional
capacities. Whether reduction of the spatial bias is sufficient, in itself, to improve
overall outcome for patients remains an open question.

INTRODUCTION
Unilateral spatial neglect is a curious difficulty in detecting, acting on or even
imagining information from one side of space that cannot be fully explained by
basic sensory loss. Numerous studies now show that its presence is associated

Correspondenc e should be sent to Tom Manly, MRC Cognition and Brain Sciences Unit,
Box 58 Addenbrooke s Hospital, Cambridge CB2 2EF, UK.
Email: tom.manly@mrc-cbu.cam.ac.uk, Tel: + 44 1223 355 294, Fax: + 44 1223 516630
This work has been supporte d by the UK Medical Research Council. I am grateful to my
colleagues , particularl y Ian Robertson and Eve Greenfield for their useful discussion s on this topic,
and to an anonymous reviewermany of whose points have been incorporated into this paper.
2002 Psychology Press Ltd
http://www.tandf.co.uk/journals/pp/09602011.html
DOI:10.1080/0960201044000101

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with grossly impaired everyday functioning and, importantly, with slowed

recovery in apparently unconnected functions, including non-spatial attention
and motor skills (Ben-Yishay, Diller, Gerstman, & Haas, 1968; Blanc-Garin,
1994; Cherney et al., 2001; de Seze et al., 2001; Denes, Semenza, Stoppa, &
Lis, 1982; Paolucci, Antonucci, Grasso, & Pizzamiglio, 2001a; Paolucci,
Grasso, Antonucci, et al., 2001b; Robertson et al., 1997; Rode, Rossetti, Badan,
& Boisson, 2001; Sea, Henderson, & Cermack, 1993). Developing and
evaluating interventions that might ameliorate the condition (or the effects of
the condition on everyday activities) are therefore important clinical aims.
Well over a thousand scientific papers on unilateral neglect have been
published in the last 20 years, many focused on the careful analysis of different
neglect phenomena and their relevance for understanding normal perception
and attention. Although there is a degree of well-justified scepticism about the
links between basic cognitive neuropsychological research and rehabilitation,
it seems almost inconceivable that at least some of these findings would not
provide useful pointers for intervention.

UNILATERAL SPATIAL NEGLECT: PRESENTATION,

AETIOLOGY, AND NATURAL HISTORY
Most readers will be familiar with the striking presentation of unilateral
neglect. Patients with apparently intact visual pathways1 may fail to find visual
targets presented on the left side of a page, may draw only the right half of a
remembered image, copy the right half of a picture, or squash the numbers from
1 to 12 into the right half of a drawn clock. They may fail to respond to auditory
stimuli originating from the left, or to tactile stimuli presented to the left limb
or the left side of a limb (Mattingley & Bradshaw, 1994). Famously, their
recollection of well-known scenes (learned prior to the injury) may be strongly
determined by their imagined point of view, omitting information on their left
that they can subsequently recall when it is imagined on the right (Bisiach &
Luzzatti, 1978). Motorically, patients may ignore their own left limbs or have
difficulty reaching to the left (Mattingley & Driver, 1996; Mattingley, Phillips,
& Bradshaw, 1994b). It is important to note, however, that patients vary enormously in the details of presentation and that neglect should not be viewed as
a unitary disorder, but rather as a cluster of deficits characterised by lateralised
spatial bias (Halligan & Marshall, 1994c; Robertson & Halligan, 1999). The
implication of this diversity for rehabilitation (i.e. whether one technique
works better for particular manifestations) is an area that has been barely

Although unilateral neglect is dissociable from visual field disorders (e.g., hemianopias ) it
should be noted that the conditions often co-occur (e.g., Hier, Mondlock, & Caplan, 1983).

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considered to dateindeed the majority of studies considered here have

primarily examined visual neglect for an area immediately in front of the
patient.
Neglect has been observed following damage to a variety of brain regions
including the parietal cortex (particularly the posterior region: Vallar & Perani,
1986), frontal cortex (Damasio, Damasio, & Chang Chui, 1980; Mesulam,
1981), basal ganglia (Bradshaw & Mattingley, 1995; Damasio et al., 1980),
striatocapsular (Chung et al., 2000), putamen (Hier, Davis, Richardson, &
Mohr, 1977), caudate (Kumral, Evyapan, & Balkir, 1999), and thalamus
(Velasco, Velasco, Ogarrio, & Olvera, 1986). Recent analyses suggest that
lesions within paraventricular white matter in the temporal lobe (Samuelsson et
al., 1997) or superior temporal cortex (Karnath, Ferber, & Himmelbach, 2001)
are most closely associated with the disorder. However, Hillis et al. emphasise
that the location and extent of clearly lesioned tissue is not always the best
predictor of disability (Hillis et al., 2000). In their study, the extent of
blood hypoperfusion within cortical regions (the ischemic penumbra), in
fact formed the better predictor of neglect. Given this diversity, neglect may
be better understood as a cluster of lateralised spatial problems that can
arise following damage toor dysfunction ina network of brain regions
and normal psychological functions involved in the allocation of attention and
representation of space (Mesulam, 1981; Robertson & Halligan, 1999).
Aspects of neglect have been reported in a surprisingly high proportion of
stroke patients within the acute phase. When assessed 23 days post-stroke,
Stone, Halligan, and Greenwood (1993) found evidence of neglect in 82% of
right hemisphere patients and 65% of left hemisphere patients (see also Stone et
al., 1991; Stone, Patel, Greenwood, & Halligan, 1992). The great majority of
patients showing this acute form of neglect apparently recover rather quickly
from the spatial biasalthough it should be noted that this is generally based on
a relatively limited range of measures (Campbell & Oxbury, 1976).
The group of patients who show more chronic forms of the disorder almost
invariably have right hemisphere lesions and neglect left space. The reasons for
this asymmetric recovery pattern remain controversial. It has been suggested,
for example, that the left hemisphere is responsible for the allocation of
attention to the right half of space, while the right hemisphere is capable
of driving attention to the left or the right (Weintraub & Mesulam, 1987).
Damage to the right hemisphere therefore leads to domination of a rightward
bias from the intact left hemisphere. The specialisation of regions of the left
hemisphere for language (homologous to those leading to neglect in the right)
has been proposed to explain this lateralityand the absence of such
asymmetries in non-human primates (e.g., Karnath et al., 2001). An alternative
view is that the right hemisphere is specialised in global processing (taking in
the whole scene) while the left is more adapted to focus on local details
(Halligan & Marshall, 1994a). Right hemisphere damage results in a focused

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attentional bias (e.g., towards right-sided targets on cancellation tasks) and

failure to detect and orient to the wider spatial context. While helping to explain
the chronic hemispheric asymmetry of neglect, these types of account are less
useful in thinking about the presence of neglect in the acute stage in many left
hemisphere patients, and the rapid recovery in some, but not all, patients with
right hemisphere damage. An alternative (although not contradictory) view
emphasises the role of damage to non-spatial right hemisphere capacities (see
below) that may form the setting conditions that allow neglect to persist
(Posner, 1993; Robertson & Manly, 1999). This account has drawn heavily on
observed differences between right hemisphere patients who recover and those
who do not (see Robertson & Halligan, 1999).
The question of how patients recover is important in thinking about rehabilitation. A number of studies suggest that some forms of apparently spontaneous
recovery may in fact reflect behavioural compensation rather than a genuine
reduction in the underlying spatial distortion. Goodale, Milner, Jakobson, and
Carey (1990) analysed the reaching trajectories of right hemisphere patients
who no longer showed neglect on standard bedside tests. Although the patients
were able to reach towards targets with a similar accuracy to that of a control
group, significant deviations into right space during the reach were still
apparent. Similarly, a bias was apparent if the patients were given the more
challenging task of pointing to the midpoint between two objects (i.e., to a
spatially-defined, rather than object-defined, region: see also Mattingley,
Bradshaw, Bradshaw, & Nettleton, 1994a). Bartolomeo (2000) compared the
performance of right hemisphere patients who currently showed neglect,
patients who had recovered from neglect, and healthy age-matched controls on
a computerised spatial task. As might be expected, while the neglect patients
produced slow or inaccurate responses to left-sided targets, the recovered
patients and the controls showed no consistent bias. When, however, the
participants were asked to perform the task while simultaneously performing a
second attentionally demanding (although non-spatial) test, a lateralised
pattern re-emerged in the recovered patients (see also Robertson & Frasca,
1992). The results suggest that, whatever the precise mechanism of behavioural
adaptation in this group (e.g., compensatory voluntary leftward eye movements: Ladavas, Carletti, & Gori, 1994) these seem to require limited capacity
top-down attentional resources. One obvious consequence of this is that
patients with co-occurring difficulties in mobilising these resources are more
likely to show chronic spatial bias.
If one difference between patients who come to effectively use compensatory strategies and those that do not is the availability of these more general
attentional/executive resourcesa useful rehabilitation approach may be to
reduce the demands of voluntary leftward scanning by making it more of a
habit. Such approaches have, to date, formed the main focus of rehabilitation
in this area.

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TRAINING LEFTWARD SCANNING AS A HABIT

Many neglect patients can become aware of a left-sided stimulus or make some
leftward eye or head movements if they are cued to do so (e.g., Riddoch &
Humphreys, 1983). The difficulty is that such cuesas with simply informing
the patient that they are missing things on the lefttend to have only very transitory effects (Halligan & Marshall, 1994b). From at least the 1960s, therefore,
therapists have tried to develop very systematic, behavioural programmes to
encourage these behaviours. Perhaps the simplest example is in the context of
reading. In reading text, neglect patients may miss the words on the left side of
each line (see Young, Newcombe, & Ellis, 1991 for discussion of other forms
of neglect dyslexia). A useful strategy is therefore to train patients to habitually find the left side of the page before attempting to read each line (i.e., using
the additional object on the left to re-frame the left side of the text line as an
object on the right). This may be assisted by using a highly salient cue (e.g., a
red book-mark) as an attentional anchor at the left of the sheetand systematically fading this cue as performance improves (Diller & Weinberg, 1977;
Weinberg et al., 1977). Such training indeed appears to be successful in
reducing left-word omissions. The problem is that very little spontaneous
generalisation seems to occur. Lawson (1962), for example, describes how a
patients improved reading was so context-specific that it did not generalise to a
different edition of the same book.
Another quite widely used technique has been to encourage patients to track
a light that moves from right into left space, with the degree of leftward
movement increasing as patients progress (Antonucci et al., 1995; Diller &
Weinberg, 1977; Pizzamiglio et al., 1992; Ross, 1992; Wagenaar et al. 1992;
Webster et al., 1984; Weinberg et al., 1977; Zihl, 2000). Again, although eye
movements during the exercise improve, generalisation has been rather
disappointing (Robertson, Gray, & McKenzie, 1988; Ross, 1992; Wagenaar et
al., 1992; Webster et al., 1984). The results appear to concord with a general
principle in rehabilitation that it is usually better to train real activities that are
useful for patients (where a lack of generalisation is less important) rather than
rely on transfer from abstract tasks (Wilson, 1996). Webster et al. (2001), for
example, have shown that training that is specific to the task of navigating a
wheelchair around complex environments produces very practical benefits.
However, as neglect permeates so many aspects of a patients life, and training
each of these activities may be beyond the resources of most services, seeking
changes in underlying function continues to be an important goal. It is
encouraging, therefore, that recent attempts at scanning training have
produced more positive results.
Pizzamiglio et al. (1992) offered patients approximately 40 hours of very
systematic, progressive training. Using a variety of tasks (including reading,
naming objects in spatial arrays, following leftward moving lights projected

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over a wide area) patients were initially given highly salient cues and therapist
encouragement to look to the left. The cues were progressively faded as awareness of left space increased. As might be expected, performance on the trained
tasks showed significant gains. Unlike previous studies, however, improvements were also noted on untrained tests and, crucially, on structured everyday
activities. The reason for these positive results (which have been replicated in a
fully randomised design: Antonucci et al., 1995) in comparison with previous
studies is unclearalthough the authors suggest that the sheer duration of the
training may have been a crucial factor.
Many neglect patients show a curious lack of awareness foror outright
denial oftheir disabilities (anosognosia). This has clear implications for their
motivation to take part in rehabilitation and their ability to detect progress. In an
interesting case study, Zoccolotti et al. (1992) have shown that the techniques
developed in Rome (Antonucci et al., 1995; Pizzamiglio et al., 1992) can
produce positive behaviour changes without necessarily effecting the patients
acknowledgement of their difficulties.
Although neglect can operate on object-based co-ordinates (the left side of
an object being neglected regardless of the objects location: Driver &
Halligan, 1991), for many patients the bodys midline appears to be a crucial
marker of what is left and what is right. A potential alternative approach to
training leftward eye movements is, therefore, to train patients to rotate their
torsos to the left in relation to their head position. In this manner, when a patient
looks straight ahead, more of the visual scene will fall to the right of the body
midline. Remarkably, this simple intervention (trunk rotated left by 15) has
been shown to significantly reduce neglect (Karnath, Schenkel, & Fischer,
1991). The difficulty is that, as with eye movements, patients are unlikely to
spontaneously make such rotations, preferring to orient the eyes, head and
trunk to the right.
The rehabilitation studies discussed so far have encouraged patients to look
(or turn) to the left during some trained activities. A different approach which,
given the difficulty in achieving generalised results, has some merit, is to essentially force patients to look to the left during all activities.

EYE PATCHING STUDIES

Butter and Kirsch (1992) explored the value of using a patch to cover the right
eye. Given that occlusion of one eye has only a marginal effect on reducing
input from one side of space (each eye having receptive fields for left and right
space), this seems, on the face of it, a rather bizarre approach. However, Butter
and Kirschs intervention was based on the proposed role of the superior
colliculi in mediating eye movements and shifts of attention. Experimental
observations have shown that the superior colliculi in each hemisphere exist in

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a dynamic relationship (activation in one hemisphere inhibits activity in the

other). Damage to one hemisphere could therefore create an uneven competition leading to a persistent orienting bias towards ipsilesional space (neglect).
Unlike the visual pathways of the cortex, each colliculus primarily receives
stimulation from the contralateral eye rather than hemifield. Preventing stimulation to the intact left superior colliculus by patching the right eye might, therefore, release the right colliculus from this competitive inhibition and allow
residual function to be better expressed (a benign form of the Sprague effect:
Sprague, 1966).
Butter and Kirsch asked 13 patients to wear right eye patches as they
performed various spatial tasks. Significant reductions in spatial bias on those
tasks were reported in 11 of the group. To potentially enhance this effect by
increasing stimulation to the right hemisphere, right eye patching was
combined with a flickering visual stimulus on the left (dynamic left-sided
visual cues had previously been shown to reduce neglect on computerised
tasks). A study of 18 patients suggested that the combination of these techniques indeed produced greater reductions in neglect than either used in
isolation.
Subsequent work has provided rather more mixed results. Walker, Young,
and Lincoln (1996) found improvements in three patients, no change in
two patients, and poorer performance in four of the patients in their study.
Barrett, Crucian, Beversdorf, and Heilman (2001) also found that right eye
patching could worsen neglect, and (in a single case study) that patching of the
left eye could, bizarrely, produce improvements. The results stress the importance of ruling out non-specific effects of interventions (e.g., heightened
arousal caused by novel proceduressee later). They may also represent a case
where one rehabilitation technique has considerable value for some patients,
while being ineffective or counterproductive for others. Further work examining which patients are likely to benefit (e.g., in terms of their presentation of
neglect, their primary lesion location, time since injury or comorbidity) is
required.
Beis, Andre, Baumgarten, and Challier (1999) examined the effect of
blocking information from the right hemifield rather than the right eye. Patients
were asked to wear glasses with the right half of each lens masked off for
approximately 12 hours a day over 3 monthsthat is well over 1000 hours.
When compared with right eye patching, the patients showed significantly
increased spontaneous eye movements to the left and, encouragingly, significant improvements in activities of daily living. The precise mechanisms of
these positive effects remain unclear. It seems likely that there is a behavioural
training effect as patients are forced to make leftward eye movements in order
to see as they perform daily activities. It is also possible that the type of effects
described by Butter and Kirsch (1992) with reference to the superior colliculus
may be in operationthat is that the intact left hemisphere, deprived of

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external stimulation, is in a poorer position to competitively suppress residual

activity in the right.

RE-DISTORTING SPACE
Prism lenses
It has been demonstrated that some of the phenomena associated with neglect
can be related to a distorted or rotated sense of ones location within space
(Karnath et al., 1991). Accordingly, researchers have examined the effect of
using interventions that, in healthy individuals, produce a similar distortion,
and using these to correct the pathological bias of neglect.
Wearing prism glasses creates an immediate distortion of space. If they are
worn for long enough, however, the brain adapts (particularly if actions
are performed). Subsequent removal leads to a refractory period during which
the perception of space (as indexed by accuracy in reaching) is distorted in the
opposite direction. In a randomised group design, Rossetti et al. (1998) asked
patients to wear prism lenses that distorted space to the rightessentially
giving them a form of hyper-neglect. After about five minutes of being asked
to make reaches towards targets, the lenses were removed. The patients showed
the adaptation effect, their straight ahead reaches now being to the left of
the pretreatment baseline. Remarkably, this brief exposure was sufficient to
improve performance on neuropsychologica l tests relative to the control group.
These improvements were still apparent when both groups were re-tested
2 hours later. Rossetti et al. suggested that the very strong error signal that
resulted from the patients observing their own inaccuracy while wearing the
prism lenses may have been sufficient to effectively re-set the perceptual/
motoric representation of space.
These positive effects have been replicated in a recent controlled study that,
in addition to using a wider range of measures, examined the persistence of the
gains at intervals up to 5 weeks post-treatment. Frassinetti et al. (2002) offered
seven right hemisphere patients with chronic neglect 20 sessions of prism
adaptation therapy (two per day over 2 weeks, each of 20 minutes duration). At
the beginning of each therapy session, before wearing the prism lenses, the
patients were asked to point to 60 visual targets presented at midline and to
the left and right of midline. Subsequently, when wearing the prism spectacles
(creating a 10 rightward shift) the patients were again asked to point to 90
central and lateralised targets. During this phase, all but the final stage of the
reaching movement was obscured from the patients sight by a box. Having
removed the prisms in the final stage of each session, the patients were again
asked to point to the targets. In this phase, all of the movement and final destination of the hand were obscured by the box. Comparison of the initial and final

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stages of each session revealed a significant leftward deviation in pointing

attributable to prism adaptation for six of the seven patients.
When compared with a pretreatment baseline, significant reductions in
neglect were apparent on Conventional and the Behavioural subtests of the
Behavioural Inattention Test (Wilson, Cockburn, & Halligan, 1987), a reading
measure (Ladavas, Shallice, & Zanella, 1997), and tasks requiring patients to
name objects located around a room and to reach for objects on a table. A trend
for improvement was also apparent on the Fluff Test (in which patients,
while blindfolded, are asked to find stickers placed on the left side of their body:
Cocchini, Beschin, & Jehkonen, 2001). These improvements were apparent at
re-tests administered two days, one week and five weeks after treatment.
Evidence in support of a specific effect of the prisms came from a control group
(based at another hospital, but otherwise matched on age, time since insult and
Behavioural Inattention Test [BIT] performance) who showed no significant
improvements despite being re-tested at the same intervals. The fact that
performance gains were also absent in the treated patient who failed to show the
normal adaptation effects to the prisms is also consistent with a rather specific
effect. Importantly, this study shows that the benefits of prism therapy are not
limited to the control of motor behaviour but appear to exert a more general,
higher level effect upon patients representation of space. If this pattern of
results is apparent in other studies, this very practical intervention should
clearly have a major impact on clinical approaches to neglect.

Optokinetic stimulation, caloric vestibular

stimulation, and neck muscle vibration
Exposure to a background display of coherently moving dots causes involuntary eye movements (nystagmus) and a distortion to the subjective midline.
Pizzamiglio et al. (1990) have shown that the performance of neglect patients
on spatial tests can be significantly enhanced by such optokinetic stimulation
although the effects appear to be broadly restricted to when the movement is
actually present. Other routes to inducing temporary subjective shifts in
midline include caloric vestibular stimulation (in which warm and cold water
are used to create a temperature imbalance between the ears: Cappa, Sterzi,
Vallar, & Bisiach, 1987; Rubens, 1985), and posterior neck muscle vibration
(thought to create a motor illusion that the head is turned: Karnath, 1994;
Karnath, Christ, & Hartje, 1993).
At first glance, the temporary nature of these effects, and the practicalities of
delivering the therapies, suggest a limited role in rehabilitation. However,
given the difficulties experienced by patients in maintaining voluntary strategies, the use of these non-volitional techniques may have valueas with visual
field patching and prism lens adaptationas part of broader rehabilitation
programmes.

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LIMB ACTIVATION
The term attention is usually used with reference to some form of limited
capacity selectionin other words mechanisms that can promote a subset of
available stimuli to dominate awareness (e.g., because they are task relevant or
inherently salient) while suppressing that which is irrelevant or unchanging. In
accounting for why a potentially highly parallel perceptual system is ultimately
reduced to a narrow channel of awareness, a number of authors have argued that
its key role lies in allowing coherent action (e.g., Allport, 1992; Rizzolatti &
Camarda, 1987). As we are generally only capable of responding to one or two
objects at a time (not least because of the limited number of limbs at our
disposal), selection is a necessary aspect of the system. In line with this
argument, our awareness of where things are may be modulated by what we
are intending to do, or what we are intending to do it with. In the context of
neglect, for example, Robertson, Nico, and Hood (1995a) found that spatial
bias could be modulated by whether a patient intended to pick up, or to point to,
an object.
The finding that has been most relevant to rehabilitation was that (at least
some) neglect patients showed marked reduction in neglect if they used their
left hands to perform a task (Halligan, Manning, & Marshall, 1990; Halligan &
Marshall, 1989; Joanette & Brouchon, 1984; Joanette, Brouchon, Gauthier, &
Samson, 1986). In a series of single case and group studies, Robertson and
colleagues (Robertson & North, 1992, 1993, 1994; Robertson, North, &
Geggie, 1992; Robertson, Tegnr, Goodrich, & Wilson, 1994a) subsequently
showed that:
1. The reduction in visual neglect did not depend on the patient being able to
see the moving left hand.
2. The left hand did not need to be performing the spatial task for the effect
to occur. Repeated finger movements of the left hand facilitated a purely
perceptual test of naming letters in a spatial array.
3. An interaction of movement of the left hand and the location of that
movement to the left of the body midline appeared to be necessary to
generate the effect (movement of the left hand in right space, or
movement of the right hand in left space did not produce significant
gains).
4. Simultaneous bi-manual movements (regardless of the location of the
hands) abolished any benefits of left hand movement on spatial
awareness.
5. Left hand movement had positive effects on cancellation tasks
performed in near (table top) and far (2.4 metres away) space, reading
tasks, walking trajectories, and tactile exploration. Subsequent research
has shown benefits for covert shifts of attention (Mattingley, Robertson,
& Driver, 1998).

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6. Although initial results in which the experimenter moved the fingers on

the patients left hand suggested that passive movements did not produce
benefitssubsequent research with larger amplitude passive movement
of the arm has reported positive results (Frassinetti, Rossi, & Ladavas,
2001)
7. Left limb activation effects have not be found in all patients (see also
Brunila et al., 2002)
The results of these studies have been useful in clarifying the potential mechanisms of the left limb activation effect. The benefits of unseen movements,
for example, clearly suggest that the effect is not simply one of visual cueing to
the left. The failure to show benefits in the bi-manual movement condition
similarly suggest that a generalised alerting (caused by the difficulty or novelty
of using the left hand) forms an unlikely account (see later for discussion of
alerting effects on neglect). If there were a simple facilitation of awareness
from intended movement in a particular location, it might be expected that
moving the right hand within left space would also produce advantages
which was not the case. It seems likely, therefore, that the additive effects of
hand and location of movement are necessary, perhaps in inducing a more
general activating effect within the right hemisphere (Robertson et al.,
1994a; see also Kinsbourne, 1993).
Many patients with neglect have dense left-sided hemiplegia. Left limb
activation is therefore unlikely to hold much rehabilitative value for this group.
For other patients, however, there may be under-use of residual function in the
left limbs for attentional reasons (motor neglect: Sterzi et al., 1993). Encouraging use of the left limb for these patients may produce benefits for both
perceptual and motor function.
Robertson et al. (1992) developed a portable neglect alert device to cue
patients to move their left hands. The device consisted of a hand-held button
which, if not pressed within a particular interval (generally around 8 s) would
trigger a buzzer. In a series of case studies using the device (Robertson, Hogg,
& McMillan, 1998a; Robertson et al., 1992), improvements across a range of
tasks (both spatial tests and everyday activities) were demonstrated. Encouragingly, for some of the patients, the improvements were well maintained
following the end of formal training. A lasting effect was also observed by
Wilson, Manly, Coyle, and Robertson (2000). Here, the patient had difficulty in
adequately completing his morning self-care routine (often failing to wash or
dress the left side of his body). Following a baseline period in which the number
of prompts required from care staff were recorded (prompts being given to
continue if activity stopped for more than 20 s before the completion of the
specified routine), the limb activation training was introduced. As with
the previous studies, this produced a quite rapid decline in the impact of neglect
on the tasks. Following 10 days of formal training, the benefits were well

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maintained for at least another 10 days, and the patient appeared to be making
more spontaneous use of his left hand. It is possible, therefore, that the
increased awareness of left space induced by the limb movement itself
promotes greater use of the left hand, establishing a beneficial feedback loop.
If patients have some movement in their left hand or arm, and if the
movement does not cause excessive discomfort, there are a number of advantages to this rehabilitation technique. Firstly, it is a very concrete activity to ask
a patient to perform, and one that is clearly observable. It is therefore possible to
get an estimate of whether it is likely to be beneficial in any given case through
looking for improvements on spatial tasks concurrent with the onset of
movement. It also lends itself to the automatic monitoring and cueing described
by Robertson et al. (1992) and to the verbal encouragement of therapists and
carers. Most importantly, it seems to lead to improvements in underlying
spatial awareness that generalise to different tasks. Beneficial effects for the
recovery of hemiplegic limbs have resulted from restraint therapy in which
the patients unaffected limbs are temporarily restrained to prevent their use
(Taub & Wolf, 1997). The value of these techniques for rehabilitation in
neglect, through encouraging greater use of the left arm, has not yet been fully
addressed.
Although many of the studies reviewed in this article have focused on a
specific technique that allows clear interpretation of positive results, this
should not be taken to imply that the best clinical outcome is likely to emerge
from the application of any of the techniques in isolation. Accordingly, Brunila
et al. (2002) recently examined the effect of combining limb activation training
with a progressive visual scanning programme. Four patients were encouraged
to move either their left arm or hand (or if that was not possible, shoulder)
during exercises including naming objects in a spatial array and cancellation
tasks. Compared with a nine week repeated assessment baseline, the 12
sessions of therapy produced significant improvements in reading, letter
cancellation and in copying a complex figure, that were well maintained over
the next 3 weeks. Again, the authors note considerable variability in the
patients response, strongly suggesting that careful evaluation of the potential
benefits of any technique for a given patient should be explored at the outset.

TARGETTING NON-SPATIAL FUNCTIONS

Right hemisphere lesions are associated with disproportionate problems with a
cluster of non-spatial attentional capacities (variously termed alerting
preparing and maintaining a ready to respond state: Benson & Barton, 1970;
Boller, Howes, & Patten, 1970; De Renzi & Fagliono, 1965; Howes & Boller,
1975; Posner, Inhoff, & Friedrich, 1987), arousal (Gainotti, 1972; Heilman,
Schwartz, & Watson, 1978), and vigilance or sustained attention (Knight,
Hillyard, Woods, & Neville, 1981; Rueckert & Grafman, 1996; Wilkins,

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301

Shallice, & McCarthy, 1987). There is, furthermore, a degree of convergence

between neuropsychologica l and functional imaging literature on the particular
importance of a right hemisphere fronto-parietal network in mediating these
functions (Knight et al., 1981; Lewin et al., 1996; Pardo, Fox, & Raichle, 1991;
Rueckert & Grafman, 1996; Sturm et al., 1999; Wilkins et al., 1987). On this
basis, it would be expected that many patients with persistent neglectwho
almost always have right hemisphere lesionswould be vulnerable to these
problems. This certainly seems to be the case. Many patients appear to be
drowsy, unresponsive and to have difficulty in maintaining their focus on any
task, regardless of its spatial content. These clinical observations have been
confirmed in experimental studies. Robertson et al. (1997) asked a large group
of patients (57 with right- and 30 with left-hemisphere lesions, mainly from
stroke), and age-matched controls, to perform a particularly tedious nonspatial
tone counting measure (Robertson, Ward, Ridgeway, & Nimmo-Smith, 1994b;
Robertson, Ward, Ridgeway, & Nimmo-Smith, 1996; Wilkins et al., 1987).
Although all patients were mildly impaired relative to the control group, it was
the right hemisphere patients with neglect who performed disproportionately
poorlyindeed it was possible to make a good guess as to which right hemisphere patients would show neglect based on the score on this test alone.
Similarly, it has been shown that neglect patients, when compared with right
hemisphere patients without neglect, have difficulty in mentally bridging the
intervals between a cue and a target in reaction time tasks (Samuelsson et al.,
1988).
Neglect is a rather volatile condition, changing in apparent severity not
simply on different tasks but on the same task at different times (sometimes to
the exasperation of experimental psychologists looking for reliable effects).
This variability is consistent with factors (such as level of arousal/alertness) not
simply being associated with neglect at a general level, but exerting a direct
modulatory influence on spatial awareness2.
This conclusion receives some support from a recent pharmacological study
in which apparently recovered stroke patients (including three patients with

2
This raises the intriguin g possibility that other groups with low levels of alertness may also
be vulnerabl e to spatial bias. In fact there is growing evidence that at least some children with the
diagnosi s of attention deficit hyperactivit y disorder (in which poor sustained attention /low
arousal are central features) may show exactly this pattern of left-sided inattentio n (Nigg,
Swanson, & Hinshaw, 1997; Sheppard, Bradshaw, Mattingley, & Lee, 1999; Loeller & Heilman,
1988) and even frank neglect on line bisection and cancellatio n tasks (Dobler et al., 2001; Manly,
Robertson, & Verity, 1997). The associato n with the adult acquired disorder and the role of low
arousal is further strengthene d by findings showing that methyphenidat e (Ritalina stimulant
medication ) can correct a bias in line bisection (Sheppard et al., 1999), and a replicatio n of
Robertson et al.s prior entry alerting interventio n in a case of developmenta l neglect (Dobler et
al., 2001).

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right hemisphere lesions) were given midazolam (a GABA antagonist) that

produces mild sedation. The period of the drugs effect (about 2 hours) was
associated with significant increases in left neglect and, interestingly, in left
hemiplegia (Lazar et al., 2002).
Robertson and colleagues examined the link between arousal and neglect
behaviourally using a prior entry computerised task. If healthy individuals
are cued to attend to the side of a display onto which two simultaneous
lateralised targets are subsequently presented, despite maintaining a central
fixation, they will tend to report the stimulus on the attended side as having
occurred firstin other words attention gives that stimulus prior entry into
subsequent processing (Stelmach & Herdman, 1991). This technique has been
used to calibrate the pathological attentional bias of neglect (Rorden,
Mattingley, Karnath, & Driver, 1996). In their study Robertson, Mattingley,
Rorden, and Driver (1998b) preceded occasional trials of the computerised task
with a loud, alerting tone. Although the tone had no predictive value for the
stimulus presentation order, its presence was associated with an abolitionor
even reversalof neglect. Heilman, Watson, Valenstein, and Goldberg (1987)
have suggested that there are two routes to developing and maintaining an
alert or ready-to-respond state. The first is exogenously driven by the
detection of intense, novel or salient stimuli. The second, suggested by reciprocal cortical projections to the brain stem, involves the internal (endogenous)
self-generation and maintenance of this state. Robertson et al.s results with
loud tones suggests that, for neglect patients, the former may be relatively intact
while the second is deficient.
Although it may be possible to use some form of external alerting during the
performance of tasks (e.g., through presenting tones or the encouragement of a
therapist of carer), as the technique appears to rely on the novelty as well as the
salience of the tones, this may not be practical as a long-term solution. Two
potential alternatives for harnessing this effect are to try and train patients in
self-maintaining an alert state during an important activity, and, given the
results of Lazar et al. (2002), to use medication that boosts rather than reduces
alertness.
Robertson and colleagues (1995b)explored the first possibility, adapting a
technique for the verbal regulation of attention first described by Meichenbaum
and Goodman (1971; see also Luria, 1963; Meichenbaum & Cameron, 1973).
During training, patients with neglect were asked to perform a number of rather
tedious tasks (e.g., sorting coins or shapes). With their prior consent, every
40 seconds or so the therapist would create a loud noise by banging the desk and
saying Attend! (or other phrase agreed with the patient). As the training
progressed, the patients would be encouraged to say Attend! themselves,
the aim being to associate this self-instruction with the sense of alertness
engendered by the loud stimulus. Subsequently, the patients were first encouraged to bang the table themselves while saying Attend!, then to simply say

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303

the phrase out loud, and finally to internalise this instruction. Although there
was no on-line monitoring (e.g., EEG) of the effect on alertness levels,
improvements in performance on a nonspatial tone-counting sustained
attention task, consistent with such enhancement, were found. Most importantly, as a group the patients showed significant improvements on a number of
untrained spatial neglect measures.

MEDICATION
In animals, behaviours analogous to unilateral neglect are associated with
disruption to the dopamine system (Corwin, Burcham, & Hix, 1996). Fleet,
Valenstein, Watson, and Heilman (1987) administered bromocriptine (a
dopamine agonist) to two patients. This stimulant was associated with
improvements in some, but not all neglect measuresimprovements that
tended to reverse when the medication was withdrawn. In a more recent case
study, Hurford, Stringer, and Jann (1998) compared the effects of methylphenidate with bromocriptine. They report that, although methylphenidate
produced benefits compared with the no-treatment condition, bromocriptine
produced the stronger results. These preliminary studies suggest that stimulant
medication may indeed have a role within rehabilitation for neglect, although
clearly larger fully controlled trials are required.

FUTURE DIRECTIONS
Although most patients who show unilateral neglect in the acute post-stroke
phase recover, the presence of chronic neglect in the less fortunate minority
is associated with slowed recovery and poor outcome. This review has considered broad approaches to the rehabilitation of neglect; training (or forcing)
leftward scanning behaviour, prism adaptation, left limb activation; and interventions designed to improve general alertness. Each has produced positive
results that have shown some generalisation to untrained tasks. It is notable, in
terms of the potential mutual benefits between cognitive neuropsycholog y and
rehabilitation, that at a number of these approaches have emerged from studies
of the underlying nature of the disorder (rather than direct treatment of the most
salient symptoms)and have furthermore raised interesting questions for
further academic study. A number of important questions, however, remain.
In order for these effects to be considered rehabilitation, it is necessary to
show firstly that the training generalises to the type of tasks that patients
actually want to perform (i.e., not simply on neuropsychological tests). This
has been evaluated in some but not all of the studies considered here. There are
several barriers to such generalisation, perhaps particularly in the complexities
and additional attentional demands of many everyday situations compared with
the single-task focus and quiet atmosphere of the testing room. The deleterious

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effects of distraction and dual tasking on apparently recovered neglect have

been elegantly demonstrated by Bartolomeo (2000). Secondly, it is necessary
to show that the effects last. The majority of studies have to date shown effects
lasting for some weeks but the longer-term consequences of the interventions
remain largely unknown.
In discussing the negative consequences of neglect on recovery and
outcome, the assumption has been that it is the neglect that is mediating this
effect. As discussed, however, neglect is associated with a cluster of other
deficits, perhaps particularly with the nonspatial attention systems of the right
hemisphere. Whether a reduction in the ostensive behavioural manifestations
of neglectwithout improvements in these other systemsis sufficient to
produce real changes in prognosis remains an open question. There is certainly
growing evidence on the role of more general executive or attentional
capacities in mediating recovery and functional adaptation following brain
injury. It may well be that improvements in our understanding of these areas
will offer new insights into the persistence and remediation of spatial and other
deficits.
In the majority of studies presented here, there has been considerable individual variation in responses to the interventions. It is also true that few of the
studies have directly contrasted one technique with another at a group level
or examined possible additive effects of combining treatments. As discussed,
neglect is a very heterogeneous condition that can arise following damage to a
variety of brain structures. While the practicalities of applying the different
approaches clearly suggests a sensible order in which to investigate their
usefulness, an experimental suck-it-and-see approach with each individual
patient remains the best policy.

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