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Brain Injury, September 2005; 19(10): 853–859

CASE STUDY

Non-declarative memory in the rehabilitation of amnesia

S. CAVACO1,3, J. F. MALEC1,2 & T. BERGQUIST2


1
Department of Physical Medicine and Rehabilitation, Mayo Clinic, Rochester, MN, USA,
2
Department of Psychiatry, Mayo Clinic, Rochester, MN, USA, and 3Centro de Estudos Egas Moniz,
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Faculdade de Medicina da Universidade de Lisboa, Portugal

(Received 2 December 2003; accepted 11 July 2004)

Abstract
The ability of amnesic patients to learn and retain non-declarative information has been consistently demonstrated in the
literature. This knowledge provided by basic cognitive neuroscience studies has been widely neglected in neuropsychological
rehabilitation of memory impaired patients. This study reports the case of a 43 year old man with severe amnesia following
an anterior communicating artery (ACoA) aneurysm rupture. The patient integrated a comprehensive (holistic) day
treatment programme for rehabilitation of brain injury. The programme explored the advantages of using preserved
For personal use only.

non-declarative memory capacities, in the context of commonly used rehabilitation approaches (i.e. compensation for lost
function and domain-specific learning). The patient’s ability to learn and retain new cognitive and perceptual-motor skills
was found to be critical for the patient’s improved independence and successful return to work.

Keywords: Basal forebrain, amnesia, non-declarative memory, rehabilitation

Introduction to develop a timetag for the separate stimuli that


they learned. In contrast to many ‘hippocampus
The basal forebrain is a heterogeneous set of type’ amnesics, basal forebrain amnesics often
telencephalic structures located immediately caudal improve their memory performance when provided
to the posterior extent of the ventral frontal lobes. with cueing. Both the basal forebrain (in the acute
These structures contain large numbers of cho- phase) amnesics and the diencephalic amnesics
linergic neurons that innervate the cortical surface. tend to confabulate. Unlike the diencephalic amne-
A critical function of the basal forebrain is to sics, the basal forebrain amnesics tend to confabulate
provide neurotransmitters such as acetylcholine to spontaneously. Despite the inability to learn new
the hippocampus and dopamine, norepinephrine declarative information, there are some forms of
and serotonin to various parts of the cerebral cortex. non-declarative memory that are spared in these
Rupture of aneurysms located in the ACoA can types of amnesic syndromes [4, 6, 7].
damage the basal forebrain. Focal damage to this Amnesic patients are usually disabled in their lives
area is known to produce anterograde amnesia for to the point of needing constant supervisory care and
declarative information [1–4]. even mild memory deficits can impact on functional
The ‘basal forebrain type’ of amnesia is known to independence. Unfortunately, there is currently
have a different pattern from the ‘hippocampus no clear way to restore lost memory functioning
type’ or the ‘diencephalic type’ [3, 5]. Patients with in patients with amnesia once the period of acute
basal forebrain amnesia are usually able to learn recovery is over. Specifically, memory retraining
separate modal stimuli, despite their inability to strategies have shown reduced efficacy in the rehabil-
learn the proper relationships and integrations of itation of patients with moderate-to-severe memory
those stimuli. These patients are also known to fail defects [8].

Correspondence: Sara Cavaco, Centro de Estudos Egas Moniz, Faculdade de Medicina da Universidade de Lisboa, Avenida Prof. Egas Moniz, 1649-035
Lisboa, Portugal. Tel: þ351217805217. Fax: þ351217942060. E-mail: sara.cavaco@mail.telepac.pt
ISSN 0269–9052 print/ISSN 1362–301X online # 2005 Taylor & Francis Group Ltd
DOI: 10.1080/01449290500109917
854 S. Cavaco et al.

Preserved non-declarative memory capacity in the low average level for both literal and semantic
amnesiacs introduces new possibilities in the fluency tasks. Screening of visual-spatial and con-
rehabilitation of these patients, i.e. in the reduction structional skills showed functioning to be within
of the effects of their handicap on their everyday func- normal range. His basic and higher order attention/
tioning. There have been some limited attempts to use concentration abilities as well as higher level execu-
skill learning methods and other non-declarative tive reasoning/problem-solving abilities were within
methods in clinical settings [9–16]. However, such the average range. Mild residual weakness was
resources still remain largely untapped. evident in cognitive processing speed/efficiency.
This case report demonstrates the contribution of During the interview, the patient showed very limited
the non-declarative memory capacity to the rehabili- insight into the impact of his impairments on his
tation of a patient with severe amnesia for declarative activities and daily life.
material due to probable basal forebrain damage. Patient’s neuropsychological profile is consistent
As indicated in previous studies [11–14], the with damage to the posterior sector of the orbito-
patient’s non-declarative memory capacity played frontal area, including the basal forebrain.
a crucial role in his successful use of external aids
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to compensate for declarative memory loss, in the Intervention


improvement of his functional independence and in
his return to work. This case report further demon- MBIOP is a comprehensive (holistic) day treatment
strates the advantage of using the vanishing cues programme, with a milieu-oriented approach to
technique to learn complex domain-specific knowle- post-acute brain injury rehabilitation [17–19]. This
dge [9] and the importance of extensive practice and individualized goal-setting programme aims to
errorless learning [16] in the amnesia syndrome. optimize the physical, cognitive, psychosocial and
behavioural functioning of people with brain injury
Case description in order to enable their community living, work and
adjustment to injury. Patient MH started the
For personal use only.

MH was a 43 years old right-handed man, with MBIOP 5 months after the neurological event
13 years of education, who developed a severe and graduated the comprehensive day programme
persistent headache. Ultimately he was diagnosed 8 months later. The MBIOP offers an integrated
with sub-arachnoid haemorrhage. He underwent and multi-modal rehabilitation. It emphasizes the
clipping of an anterior communicating artery importance of community education, the importance
(ACoA) aneurysm. Subsequently, he underwent providing and receiving feedback from others and
multiple surgeries for hydrocephalus, including left the importance of self-evaluation based on indivi-
frontal ventriculostomy. Due to the clipping it was dualized goals to enhance the self-awareness and the
not possible to obtain an MRI nor perform a detailed sense of involvement in the rehabilitation process.
anatomical analysis. However, ruptures of the ACoA The importance of using the patient’s preserved
aneurysms are known to damage primarily the basal non-declarative memory capacities was most notice-
forebrain. able on the rehabilitation of memory impairment and
return to work. This report focuses on these two
Neuropsychological assessment major areas of intervention.
Patient MH was first evaluated by the Mayo Brain
Injury Outpatient Programme (MBIOP) 5 months Memory impairment
after the clipping. At that time, the patient’s The memory rehabilitation process of patient
neuropsychological profile was most notable for the MH focused primarily on compensation for lost
presence of significant deficits in learning and function and substitution of intact function. These
memory for both visual and verbal information, as two approaches target disability (i.e. the lack of
demonstrated by the patient’s performance on the ability to undertake an activity at a normal level)
Wechsler Memory Scale III (WMS-III), the Visual rather than impairment (i.e. lack of a body part or
Spatial Learning Test and Rivermead Behavioural function) and attempt to achieve specific functional
Memory Test (Table I). During interviews and outcomes (Table II).
spontaneously the patient showed confabulatory
tendencies.
Compensation for lost function
The neuropsychological assessment reflected
verbal and non-verbal intellectual abilities within Use of external aids. The efficient use of a notebook
the lower portion of the average range. In language to compensate for MH’s memory impairment was
functioning, the patient showed normal performance believed to be of major importance for his functional
in visual naming and auditory comprehension. independence. The training on the use of the
Verbal fluency performance was slightly weaker, at notebook was based on the method proposed
Non-declarative memory in the rehabilitation of amnesia 855

Table I. Neuropsychological test results for patient MH.

Tests Scores

WAIS-III
Verbal IQ 97
Performance IQ 86
Full scale IQ 91
Verbal comprehension 93
Perceptual organization 91
Working memory 90
Processing speed 84
COWAT 30 (12–22%ile)
Category fluency 32
MAE naming 58
MAE token 44 (82%ile)
WRAT3 arithmetic SS ¼ 100
WMS-III
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Word list—immediate 4/5/6/6


Delayed 0 (0% retention)
Logical memory—immediate 14
Delayed 2 (14% retention)
Visual reproduction—immediate 48
Delayed 17 (35% retention)
Visual spatial learning test
Designs 18 (SS ¼ 3 in reference to a 61 year old)
Errors 4 (SS ¼ 10 in reference to a 61 year old)
Design and position 2 (SS ¼ 2 in reference to a 61 year old)
Rivermead behavioural memory test 1/12
Wisconsin card sorting test
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Number of categories 6
Perseverative responses 12 (T score ¼ 51)
Perseverative errors 12
Category test (Russell’s short form) T score ¼ 42
Trail making test
A 2700 (T score ¼ 50)1
B 6700 (T score ¼ 47)1
Beta mazes SS ¼ 8
Beck depression inventory 7
1
According to the Mayo’s Older Americans Normative Studies (MOANS) standards.

by Sohlberg and Matter [20]. The training process and photographs to compensate for his memory
went through three major phases: acquisition, impairment. Rapidly it was clear that these external
application and adaptation. Based on the patient’s aids were neither adequate nor efficient, because
accomplishments and consolidation of target behav- the patient frequently failed to carry these aids.
iours, the level of demands from phase-to-phase After a small period of assessment of the patient’s
increased progressively. With the patient’s inability needs, he was recommended to use a pocket-size
to use declarative memory functions, it was believed notebook composed of a 2-page-per-day planner,
his training on the use of the memory notebook had specific sections (e.g. medical section, vocational
to rely heavily on non-declarative memory functions. section, telephone section, family section) and cue
As a consequence, during the training, the number cards (i.e. reminders of important information
of repetitions that MH needed to learn and the designed to be quickly accessible).
amount of time the patient spent on each phase were A significant part of the rehabilitation team’s
inevitably higher than other patients with less efforts were focused on training detailed recording
declarative memory impairment that have partici- of information in the notebook. People without
pated in the programme. The training was based on memory problems are often able to retrieve the
extensive practice, cueing and feedback. necessary information from minimally detailed
The size and composition of the external aids notes, because supported by their episodic memory
are important aspects for its adequate and efficient they can fill the missing parts and reconstruct the
use. Upon admission to the programme, the patient message. When a patient has memory impairment
used both a pocket-size month-at-a-glance planner for episodic information, the quality of the notes
and a large notebook of personal information on the notebook becomes a central point.
856
S. Cavaco et al.
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Table II. Rehabilitation of memory.

Memory rehabilitation approaches Rehabilitation methods Specific techniques Goals Applications

Restoration of damaged function—attempts to Practice and rehearsal Meaningful or elaborative rehearsal, Achieve general mnemonic benefits Learn specific pieces of
restore damaged memory processes; targets distributed practice, over-learning, information
underlying impairment spaced retrieval
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Optimization of residual function—attempts to Mnemonic strategies Visual imagery, verbal organization Achieve general mnemonic benefits Learn arbitrary associations,
retrain normal memory processes; targets and association strategies, including or learn specific information sequences of actions and text
underlying impairment story mnemonics, first-letter cueing,
chaining and PQRST
Compensation for lost function—compensates Environmental supports and Labels, instructions, notebooks, Solve everyday memory problems Assist in independent living
for or bypasses memory deficits; targets external aids diaries, calendars, alarm watches, and in prospective memory
functional deficits timers, electronic organizers, pagers
Substitution of intact function—uses intact Domain-specific learning Vanishing cues, errorless learning Learn specific knowledge relevant Learn skills or tasks that can be
memory processes to substitute for damaged in everyday life performed implicitly
ones; targets functional deficits
1
Based on Glisky and Glisky [22].
Non-declarative memory in the rehabilitation of amnesia 857

Patient MH had to learn important procedural Domain-specific learning


organizational skills. He was trained to record
Vanishing cues and errorless learning. The ability to
daily information (e.g. appointments, assignments)
learn depends on the capacity to correct errors based
according to six major questions, i.e. what, when,
on prior experience. Patients with declarative
where, who, why, how. Besides the content, the
memory impairment are particularly vulnerable to
patient was also trained to record information
errors. Declarative memory has a crucial role in the
following a location outline (e.g. scheduled appoint-
correction of performance based on the feedback of
ments should be recorded next to the appropriate
prior learning episodes. Non-declarative memory
time, work assignments should be recorded on the
‘appears to be typically based on emitting the
right side page). The consistency of these procedures
strongest response, and if that response is an
is believed to facilitate the efficient retrieval of
erroneous response, then the error is likely to be
information.
further strengthened’ [16 page 53].
The accurate recording for future reference also
To increase the potential for successful learning of
depends on the adequate management of the avail-
new skills, the programme promoted (especially in
able space. In addition to procedural organizational
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the early phase of intervention) an errorless learning


skills, the patient had to acquire the perceptual-
motor skill of writing clearly all the necessary environment (i.e. environment that prevents the
information on a restricted space. patient from making mistakes during learning)
In addition to recording planned tasks and based on the vanishing cues technique. So, patient
activities, it was important for the patient to learn MH was provided with external cues to avoid
the routine of checking off as soon as the tasks errors during learning. This goal was not always
were completed and to record a summary of what achieved due to the outpatient characteristic of the
he had just done for future reference. This type of programme. The frequency and detail of cues were
information is of critical importance for the patient’s progressively adjusted to the patient’s needs.
sense of accomplishment and continuity, as well as to Based on the detailed evaluation of MH’s indivi-
For personal use only.

document task completion for future reference. dual needs, he and the staff within the first month
MH was able to slowly transfer these learned skills developed some specific long-term treatment goals
to the working setting. The routine of recording (e.g. I will use my planner and fact sheet throughout
information and referring to it on a regular basis the day to compensate for my memory so I can get
appeared to be a key factor in job performance. things done efficiently). These long-term goals were
then broken down in small behaviour anchors,
Environmental supports. Acknowledging that the i.e. short-term goals (e.g. ‘with 0–1 direct cues,
environment where MH lived and worked could I will write specific details to remember information
potentiate or jeopardize his improvements, the staff on the right page of my planner’). Attending to MH’s
considered it critical to intervene thoroughly in the achievements and/or difficulties, the amount and
environment. The family, other supportive people quality of cueing aimed on the short-term goals
involved in his life and the employers were educated were periodically reviewed and gradually reduced
about his significant memory difficulties, his dimini- by the patient and the staff throughout the
shed awareness, on the use of cueing techniques and programme.
the importance of structure and routine.
The patient underwent a complete change of Return to work
wardrobe in order to accommodate the consistent
transport of the notebook. New pants with pockets From the beginning, the patient identified as his
of the size of the notebook facilitated the acquisition most important personal goal to return to work.
of the behaviour of picking the notebook from the A comprehensive and individualized return-to-work
pocket to record and/or retrieve information every plan was developed for him. The programme’s
time it was necessary. It also facilitated the acquisi- vocational service addressed patient’s functional
tion of the behaviours of reliably placing the note- limitations, helped him to identify realistic goals
book in the pocket and carrying it everywhere and bridged the gap between hospital and
(including leisure situations). As an example, the community services.
patient’s tendency to confabulate about the cause Patient MH like any person with moderate-to-
of his brain injury was addressed with a ‘fact sheet’ severe memory impairment for declarative informa-
placed on the first page of his notebook. The patient tion was hindered from performing certain types
was trained to refer to it every time he had to of work that required continuous tracking of new
introduce himself to a visitor. The automatization information. Some jobs may prove to be too
of this behaviour was rapidly acquired through the challenging or too hazardous for someone with
method of vanishing cues. amnesia. This was the case for the job that MH
858 S. Cavaco et al.

had before his injury. Prior to his injury, he had a When the patient entered the programme he was
stable working history, operating his own business not working, rating 1 on the five points’ Vocational
as a landscaper and logger for 20 years. Independence Scale [21]. At discharge and at
Despite his defective acquisition, retention and 2 months follow-up the patient was working part-
retrieval of new declarative information, he was able time in a community-based job with permanent
to successfully learn to perform some jobs that relied support, rating 3 on the same scale. Despite working
heavily on non-declarative information. at a competitive level, he still needed a permanent
Six months after the beginning of the programme, job coach support.
the patient started the vocational evaluation with a Upon admission to the programme the patient
5 week centre-based situational assessment, followed lived with his relatives and required extensive super-
by a community based situational assessment. vision. At completion of the programme and at
The rehabilitation process benefited from the 2 months follow-up the patient was independent
patient’s high motivation to work and his natural with his self-cares and living in Adult Foster Care.
interest on physical labour. He fully engaged on all He still required moderate assistance with managing
sheltered workshop-based and community-based responsibilities of independent living (e.g. meet
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vocational evaluations (e.g. ‘sort, pack and prepare transportation needs, manage money and finances).
forensic kits for shipping’; ‘operate a commercial
dryer’; ‘sort, fold and pack laundry’). All these job Discussion
trials relied heavily on cognitive and perceptual-
motor skill learning through extensive practice with The distinction between declarative and non-
little demands on episodic learning. Two months declarative memory systems was clearly demon-
after discharge, the patient was still working in a strated in this case. MH showed preserved capacity
nursery garden department store. The patient was to acquire and retain new procedures, while demon-
adequately performing this job (i.e. unload, water, strating significant declarative memory impairment.
Patient MH’s severe memory dysfunction interfered
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dispose of dead leaves and display plants in a nursery


garden department store) and expressed his wish substantially with his ability to function adequately
to pursue his vocational career in this area. in a broad range of day-to-day activities. However,
The work setting called the patient to transfer and it was demonstrated that it is possible to improve
apply the skills (e.g. efficient use of cue cards to patient’s quality of life and independence by using
perform tasks and to organize other aspects of the unaffected cognitive functions.
work-site, such as locations and co-workers names) Vocational success and functional independence
and compensation techniques (e.g. stop and think, are two of the most important measures of brain
double-check) learned in the programme. The joint injury rehabilitation. Vocational success was MH’s
effort of hospital and community-based services most important personal goal. The patient’s
vocational reintegration plan was based on his
and employers helped the patient to transfer the
personal interests and preserved capacities. To
skills learned in the clinical setting to a job in the
meet the demands of vocational functioning (e.g.
community. As a result he was able to perform all
job performance, interacting in the working setting
duties as assigned and his productivity was within
and transportation needs) and functional indepen-
expectations of competitive employment.
dence, patient MH had to learn and relearn new
skills.
Evaluation of the rehabilitation process The patient acquired most of the required cogni-
tive and perceptual-motor skills. These skills reached
The Mayo-Portland Adaptability Inventory 3.0 the automated level after extensive repetition of
(MPAI) is a measure of long-term (post-acute) target behaviours. Most target behaviours were
outcome of acquired brain injury. This inventory associated with an adequate use of external aids.
was completed on the patient’s admission and The repetition of these behaviours was supported
discharge of the programme by consensus of the by an errorless learning environment based on the
evaluation team. Upon admission, patient MH progressive reduction of cues (i.e. vanishing cues
received a total MPAI score of 44 points and at technique).
discharge a score of 38 points. Both of these scores The adequate use of external aids (e.g. planner,
indicated that the patient presented moderate overall cue cards) had a crucial role in MH’s return to
limitations related to his brain injury. The improve- work. To optimize the rehabilitative power of this
ments were on independence of self-cares, level of training, the work settings were specifically prepared
initiation, frequency of social contacts beyond family to deal with a worker with memory impairment. As
and professionals, involvement with leisure and a result, the patient learned to perform some jobs
recreational activities and work situation. and maintain an adequate working situation, which
Non-declarative memory in the rehabilitation of amnesia 859

had a significant positive impact on his sense of 8. Sohlberg MM, Mateer CA. Cognitive rehabilitation: An
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