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Cognitive deficits after traumatic coma
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From Philippe Azouvi, Claire Vallat-Azouvi and Angelique Belmont, Cognitive deficits after traumatic coma.
In: Steven Laureys, Nicholas D. Schiff and Adrian M. Owen, editors: Progress in Brain Research, Vol 177,
Coma Science: Clinical and Ethical Implications, Steven Laureys, Nicholas D. Schiff and Adrian M. Owen.
The Netherlands: Elsevier, 2009, pp. 89–110.
ISBN: 978-0-444-53432-3
© Copyright 2009 Elsevier BV.
Elsevier
Author's personal copy
S. Laureys et al. (Eds.)
Progress in Brain Research, Vol. 177
ISSN 0079-6123
Copyright r 2009 Elsevier B.V. All rights reserved
CHAPTER 8
Cognitive deficits after traumatic coma
Philippe Azouvi1,2,4,�, Claire Vallat-Azouvi3,4 and Angelique Belmont1,4
1
AP-HP, Department of Physical Medicine and Rehabilitation, Raymond Poincare Hospital, Garches, France
2
University of Versailles-Saint Quentin, France
3
UGECAM-antenne UEROS, Raymond Poincare Hospital, Garches, France
4
Er 6, UPMC, Paris, France
Abstract: Survivors from a coma due to severe traumatic brain injury (TBI) frequently suffer from longlasting disability, which is mainly related to cognitive deficits. Such deficits include slowed information
processing, deficits of learning and memory, of attention, of working memory, and of executive functions,
associated with behavioral and personality modifications.
This review presents a survey of the main neuropsychological studies of patients with remote severe TBI,
with special emphasis on recent studies on working memory, divided attention (dual-task processing), and
mental fatigue. These studies found that patients have difficulties in dealing with two simultaneous tasks, or
with tasks requiring both storage and processing of information, at least if these tasks require some degree
of controlled processing (i.e., if they cannot be carried out automatically). However, strategic aspects of
attention (such as allocation of attentional resources, task switching) seem to be relatively well preserved.
These data suggest that severe TBI is associated with a reduction of resources within the central executive
of working memory. Working memory limitations are probably related to impaired (i.e., disorganized and
augmented) activation of brain executive networks, due to diffuse axonal injury. These deficits have
disabling consequences in everyday life.
Keywords: traumatic brain injury; cognition; memory; attention; working memory; executive functions
disability in survivors from a severe traumatic brain
injury (TBI). These deficits are a complex combination of slowed information processing, of deficits
of long-term memory, of working memory and
attention, of executive functions, and of personality
and behavioral changes. They are mainly the
consequences of diffuse axonal injury. They have
a profound impact on family interactions (Brooks,
1984), social and recreational life (Oddy et al.,
1985; Tate et al., 1989), vocational reintegration
(Dikmen et al., 1994; Ponsford et al., 1995b), and
quality of life (Mailhan et al., 2005; Webb et al.,
1995). This review addresses the main cognitive
deficits experienced by patients who survive from a
Introduction
Survivors from a traumatic coma frequently suffer
from lifelong disability. For example, in a population-based study, Masson et al. (1996) found that,
five years post-injury, 44.4% of survivors had a
moderate disability, and 14.4% a severe disability,
according to the Glasgow Outcome Scale (GCS).
Cognitive deficits are the main cause of long-lasting
�Corresponding author.
Tel.: +33 1 47 10 70 74; Fax: +33 1 47 10 70 73;
E-mail: philippe.azouvi@rpc.aphp.fr
DOI: 10.1016/S0079-6123(09)17708-7
89
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coma due to a severe TBI, with special emphasis
on recent findings of limitations of central executive functions after TBI. Severe TBI is usually
defined by a score of 8 or less on the GCS, and/or
by a post-traumatic amnesia (PTA) duration of
seven days or more. However, a few studies
covered in the present review also included
patients with moderate TBI, as defined by a GCS
score 9–12, and a PTA of 1–7 days. Mild TBI (GCS
13–15, PTAo24 h) will not be addressed in this
review, as it is usually associated with a very brief
loss of consciousness and raises quite different
methodological and scientific issues. An Appendix
Table A1 at the end of the paper summarizes the
main results of cognitive testing after TBI that are
presented in this review
Long-term memory
After emerging from coma and vegetative state,
TBI patients usually pass through a phase of
global cognitive disturbance, generally termed
post-traumatic amnesia (Russel and Smith,
1961). Patients with PTA have regained consciousness, but remain confused, disoriented for
time and place, unable to store and retrieve new
information; some degree of retrograde amnesia
is usually present as well. Recovery is usually
gradual, beginning with orientation for the person
(name, age), followed in 70% of cases by
orientation for place, then ultimately for time
(High et al., 1990). The consistent return to
continuous memory indicates clearing of PTA.
However, memory problems frequently persist
after the period of PTA. Memory impairment is
one of the most frequent complaints from patients
and their relatives after a severe TBI (Brooks et al.,
1986; Oddy et al., 1985; Van Zomeren and Van den
Burg, 1985). Brooks et al. (1987) reported that
memory deficit was significantly correlated with the
inability to return to work seven years post-injury.
However, memory is not a unitary system. Longterm memory is usually considered as composed of
different cognitive subsystems, which will be
addressed in the following sections. Short-term
memory will be considered separately, as it is
closely related to executive and attention functions.
Anterograde episodic memory
Anterograde long-term episodic memory has
been one of the most extensively studied domain
(for a recent review see Vakil, 2005). This term
refers to the ability to acquire new information.
Patients with severe TBI perform poorer than
controls on all types of memory tasks, such as
paired-associates (learning of pairs of words), free
recall (either immediate or delayed), cued recall
(recall after providing a cue, such as the semantic
category), and recognition (Baddeley et al., 1987;
Bennett-Levy, 1984; Brooks, 1975, 1976).
Although visual memory has been less investigated, it seems to be impaired to a comparable
extent with verbal memory (Brooks, 1974, 1976;
Hannay et al., 1979). Zec et al. (2001) investigated
the very long term effect of severe TBI (at an
average of 10 years post-injury) with standardized
index scores from the Wechsler memory scalerevised (WMS-R) that allows a comparison with
well-established norms. The mean scores after
very severe TBI were below 1 SD of the norms for
all long-term memory indexes (verbal memory,
visual memory, general memory, and delayed
recall). Patients also tend to produce more
intrusions (words not belonging to the list they
had learned) than controls (Crosson et al., 1993).
There are at least three stages of information
processing in episodic memory: encoding (acquisition of new information), consolidation (maintaining a memory trace), and retrieval (recovery
of stored information either through recall or
recognition processes). Whether these different
processes could be selectively impaired after TBI
is a matter of debate (Vakil, 2005).
Learning rate can be assessed with multiple
repeated trials of information presentation. Most
studies found that the learning rate (i.e., increase
in the number of items correctly recalled across
successive trials) of patients with severe TBI was
slower compared to that of controls (Crosson
et al., 1988; DeLuca et al., 2000; Haut and Shutty,
1992; Levin et al., 1979; Novack et al., 1995; Shum
et al., 2000; Zec et al., 2001), although a few
studies reported opposite results (Shum et al.,
2000; Vanderploeg et al., 2001). Patients with
severe TBI required more learning trials than
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controls in order to reach the same level of
performance (DeLuca et al., 2000). TBI patients
also showed inconsistent and disorganized learning with a greater turnover of words from one trial
to the other, as compared to controls (Levin et al.,
1979; Paniak et al., 1989).
Semantic encoding can be assessed by different
methods. Vakil et al. (1992) found that the recall
of a short story after a long delay (until one day)
was not significantly influenced in patients with
TBI, by the relative importance of the information
in the story: contrary to controls, patients did not
show a better retention of the most important
items. When lists of words belonging to different
semantic categories were presented in a random,
nonclustered order, patients exhibited less semantic clustering than controls (Crosson et al., 1988;
Levin and Goldstein, 1986). In contrast, if the
words were presented in a clustered order (i.e.,
grouped according to their semantic category),
their performance improved like that of controls.
Patients were able to benefit from semantic
encoding, but to a lesser extent than controls
(Goldstein et al., 1990). These results suggest that
patients with TBI have a reduced ability to
spontaneously use active or effortful semantic
encoding to improve learning efficiency, but that
they are able to benefit from externally provided
semantic organization (Levin, 1989; Perri et al.,
2000; Vakil, 2005).
Patients with TBI are able to benefit from
memory aids such as cued recall or recognition.
Under the cued recall condition, patients are
given a cue (usually the semantic category) that is
assumed to facilitate memory retrieval. Recall of
patients with severe TBI has been found to be
significantly improved by semantic cues (Crosson
et al., 1988; Vakil and Oded, 2003). Vanderploeg
et al. (2001) found that TBI patients demonstrated comparable benefit from semantic and
recognition retrieval cues as compared to controls
(Vanderploeg et al., 2001).
The generation of mental images is an efficient
method to improve learning. Richardson and colleagues (Richardson and Barry, 1985; Richardson,
1979) found that patients with minor head
injury were impaired as compared to controls
in the recall of concrete but not abstract words.
This difference disappeared when subjects were
instructed to use mental imagery for improving
encoding efficiency, a finding also reported by
others (Twum and Parente, 1994). This finding
was interpreted as a failure to construct spontaneously interactive images for improving encoding efficiency.
TBI has been found associated with an accelerated forgetting rate, and with a most profound
deficit for delayed as compared to early memory
indexes, suggesting a consolidation deficit
(Carlesimo et al., 1997; Crosson et al., 1988; Hart,
1994; Haut and Shutty, 1992; Haut et al., 1990;
Vanderploeg et al., 2001; Zec et al., 2001). This
seems to be true even after equating baseline
initial acquisition of information (Hart, 1994;
Vanderploeg et al., 2001).
A few studies assessed sensitivity to interference after TBI. The basic principle is to present
successively two lists of words (A and B), and to
assess whether the first list interferes with learning
of the second (proactive interference) or whether
the second list interferes with later recall of the
first list (retroactive interference). Patients with
TBI were found to be more vulnerable than
controls to retroactive interference but not to
proactive interference (Crosson et al., 1988;
Goldstein et al., 1989; Shum et al., 2000).
The degree of impairment may vary quantitatively from one patient to the other (Haut and
Shutty, 1992). A minority of patients suffer from a
dense amnesic syndrome, comparable to that
observed after diencephalic amnesia (Levin,
1989; Levin et al., 1988a). The majority of patients
present less severe impairments. But qualitative
differences may also exist. Subgroups of patients
characterized by different learning strategies have
been identified by means of cluster analysis with
subscores from the California Verbal Learning
Test (CVLT) (Deshpande et al., 1996; Millis and
Ricker, 1994): active (impaired unassisted retrieval but with active encoding strategies and
preserved ability to store novel information),
passive (over-reliance on serial position of words
in the list), disorganized (inconsistent, haphazard
learning style), and deficient (the most impaired,
with a slow acquisition rate, passive learning style,
and rapid forgetting). Cluster analysis with CVLT
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has also been used to determine whether memory
disorder subtypes within TBI correspond to
deficits in underlying conceptualizations of memory constructs (Curtiss et al., 2001). Three
subgroups were identified, corresponding to specific disorders in consolidation, retention, and
retrieval processes. No cluster was identified
corresponding to encoding problems (Curtiss
et al., 2001).
Retrograde memory
Retrograde amnesia is the loss of memory of
events experienced prior to injury, involving the
individual’s experiences (autobiographical memory), memory for public events, and semantic
knowledge. Although such disorders may affect
social adjustment and the resumption to normal
life, they have received little attention. Individual
case reports of disproportionate impairment
of retrograde memory has been reported
(Markowitsch et al., 1993; Mattioli et al., 1996).
A high prevalence of retrograde memory deficits
has been reported after TBI, encompassing both
the domains of autobiographical and public events
memories, and also early acquired basic and
cultural knowledge (Carlesimo et al., 1998). Levin
et al. (1985) found evidence of partial retrograde
amnesia for episodic memories of no personal
salience (titles of television programmes) during
and shortly after the resolution of PTA, without
any temporal gradient (i.e., earliest memories
were not selectively preserved). In a recent study,
chronic (W1 year) TBI patients were found
significantly impaired in recalling autobiographical episodes and spatio-temporal details, without
any temporal gradient (Piolino et al., 2007).
Interestingly, deficits involved not only the
ability to recall memories, but also the ability to
mentally travel back through subjective time and
to re-experience or relive the past (autonoetic
consciousness). In addition, patients also had
impaired ability to use a mentally generated
image with a subjective point of view similar to
that of the original episode (self-perspective).
These disorders were significantly correlated with
tests of executive functions, suggesting that they
might be related to frontal dysfunction (Piolino
et al., 2007).
Prospective memory
Prospective memory involves remembering to
perform a previously planned action at a given
time (time-based), or after a predetermined event
has occurred (event-based prospective memory).
Although little research has been carried out in
this field, all studies found evidence of deficits of
both time-based and event-based prospective
memory after TBI (Groot et al., 2002; Kinsella
et al., 1996; Shum et al., 1999). The mechanisms of
prospective memory deficits after TBI remain to
be elucidated. A relationship with episodic
memory has been reported (Kinsella et al.,
1996), while another study found that poor
performance was related to impaired executive
functions (Kliegel et al., 2004).
Other aspects of memory
Implicit memory refers to the unconscious expression of memories. Implicit memory is inferred
from changes in the efficiency or the accuracy with
which an item is processed when it is repeated,
independently of conscious (explicit) memory of
this item (Moscovitch et al., 1994). It is operationally assessed by priming effects. Procedural
memory refers to acquisition of a general cognitive or sensorimotor skill. Data on implicit
memory and procedural learning after TBI are
contradictory (for a review, see Vakil, 2005).
Implicit memory could be relatively preserved
after TBI, but only for tasks that can be processed
relatively automatically.
Additional difficulties have been reported after
TBI in recalling the temporal sequence of the
information (Vakil et al., 1994) and the frequency
of occurrence of items in a series (Levin et al.,
1988b) and in attributing proper source to a
familiar event (source memory) (Dywan et al.,
1993).
In summary, although it is clear that survivors
from a traumatic coma suffer from long-lasting
deficits of long-term episodic memory, the
mechanisms underlying such deficit remain
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debated. Also, it is not clear whether other aspects
of memory (implicit memory, procedural learning) are impaired. In many aspects, memory
impairments after TBI seem closely related to
attentional and executive impairments, and
resemble the kind of memory disorders found
after frontal lobe lesion. For example, difficulty in
applying active or effortful strategy in learning,
the deficient use of semantic encoding, susceptibility to interference, and poor temporal and
contextual memory have been reported both after
TBI and with other focal prefrontal lesions
(Shimamura et al., 1991).
Working memory
Theoretical aspects
The concept of working memory has replaced
the older concept of ‘‘short-term memory’’
(Baddeley, 1986). Working memory is as a system
used for both storage and manipulation of
information, hence playing a central role in
complex cognitive abilities such as problem
solving, planning, language, and more globally in
nonroutine tasks (Baddeley, 1986). According to
the Baddeley and Hitch model, working memory
is assumed to be divided into three subsystems
(Baddeley and Hitch, 1974; Baddeley, 1986). The
central executive is an attentional control system,
while the phonological loop and the visuo-spatial
sketchpad are two modality-specific slave systems
responsible for storage and rehearsal of verbal
and visuo-spatial information, respectively. The
central executive functions to coordinate and
schedule mental operations. It has a limited
capacity and also serves as an interface between
the two slave systems. The central executive is
assumed to be a control system, very close
conceptually from executive functions.
Case studies
A few individual case reports of TBI patients
suffering from a selective impairment of the
central executive have been reported. Van der
Linden et al. (1992) reported the case of a 29-year
old man examined one year after a severe TBI
with left prefrontal contusion. This patient complained of difficulties in his work, particularly for
reading and understanding complex technical
texts. Neuropsychological assessment showed
preserved long-term memory and executive functions. He was found however to suffer from a
selective deficit of the central executive of working memory, as indicated by low verbal and
nonverbal spans, and an impairment of shortterm memory tasks with interference. In these
latter tasks, known as the Brown–Peterson paradigm (Brown, 1958; Peterson and Peterson, 1959),
patients are required to recall trigrams of items
(usually consonants, but visual stimuli can also be
used) after short delays (ranging from 3 to 20 s).
During the delay, different interfering tasks can
be used to prevent subvocal rehearsal of information (either simple articulatory suppression by
repeating aloud phonemes such as ‘‘ba-ba,’’ or
more complex tasks such as backward counting
and mental calculation). This patient was profoundly impaired in Brown–Peterson tasks, particularly when complex interfering tasks were used.
Two case studies of patients with remote (more
than 30 months post-injury) severe TBI and
relatively isolated deficit of the central executive
of working memory have also been reported
recently (Vallat-Azouvi et al., 2009).
Experimental studies
There have been only few studies that systematically addressed the different subcomponents of
working memory in survivors of a severe TBI.
Brooks (1975) used the digit span task. Subjects
were required to recall a series of digits, either
forwards or backwards. He found that severe TBI
patients did not differ from controls on forward
digit span, but performed significantly poorer on
backward digit span. Stuss et al. (1985) assessed a
group of 20 patients with various degrees of injury
severity, which had an apparent good recovery
but yet continued to have persistent complaints
more than two years after the injury. Patients
received a comprehensive battery of neuropsychological tests. On multivariate analysis, the test
that best discriminated patients from controls was
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n-back task in patients with remote severe TBI.
We found a load-dependent deficit, with a
decrement of accuracy (percentage hits) under
the 2-back condition (Fig. 1) (Asloun et al., 2008).
Similar findings were reported in children with
severe TBI (Levin et al., 2004; Newsome et al.,
2007).
Random item generation requires individuals to
spell out a sequence of items (letters or numbers)
as close as possible as a random series (i.e., like
drawing numbers or letters from a hat, one at a
time, calling them out, then replacing them,
so that on any draw any of the stimuli was
equally likely to be selected). It has been shown
(Baddeley, 1966, 1986) that the ability to
generate pseudo-random series depends on a
limited-capacity response selection mechanism,
similar to the central executive system. Random
generation requires the constant inhibition of
routine procedures, the ability to generate new
retrieval plans, and the rapid shifting from one
strategy to another. We used random generation
in a series of studies (Azouvi et al., 1996, 2004;
Leclercq et al., 2000). In a first study (Azouvi
et al., 1996), patients had to generate 100 letters at
an externally paced rate (every 1, 2, or 4 s). As
compared to controls, patients’ randomness
indexes were poorer and deteriorated more
with increasing generation rate (Fig. 2). In
two subsequent studies on patients, at a
100
90
% hits
the Brown–Peterson paradigm of short-term
memory with interference, described earlier
(Stuss et al., 1985).
The Paced Auditory Serial Addition Test
(PASAT) has been widely used to assess speed
of information processing and working memory
after TBI (Gronwall and Wrightson, 1981;
Gronwall, 1977). This task requires the subject
to add pairs of digits presented at a predetermined
rate. After each digit, the subject has to give the
sum of that and the immediately preceding digit.
This task is assumed to tap different cognitive
functions, such as sustained attention and working
memory, but also to be strongly related to speed
of processing. Information processing speed, as
assessed with the PASAT, was significantly
reduced one year after a severe TBI (Levin
et al., 1990). However, patients’ performance
did not decrease significantly more than that of
controls when increasing stimuli presentation rate
(Ponsford and Kinsella, 1992; Spikman et al.,
1996). This suggests that performance in the
PASAT may be more dependent on processing
speed than on working memory.
In the n-back task, subjects are presented at a
regular rate string of stimuli (letters, digits, figures
etc.), either visually or auditory, and are required
to decide whether each stimulus matches a
predetermined target (Asloun et al., 2008). The
0-back (control) condition has a minimal working
memory load: individuals are asked to decide
whether the current stimulus matches a single
predetermined target, which is always the same
throughout the task. During the 1-back condition,
individuals are asked to decide whether the
current stimulus matches the previous one.
The 2-back condition requires a comparison of
the current stimulus with the one that had been
presented 2-back in the sequence. The n-back task
allows the opportunity to assess the effect of
parametrically increasing working memory load
without any other modification in task structure.
Perlstein et al. (2004) used a visually presented
letter n-back task. They found that patients with
moderate and severe TBI were impaired, in terms
of performance accuracy, but not in terms of
speed of responding only in the more demanding
2- and 3- back conditions. We also used a letter
80
70
Controls
60
TBI
50
0-back
1-back
2-back
Fig. 1. n-back task. Data are the percentage of hits (targets
successfully identified) under 0-, 1-, and 2-back condition. TBI
patients’ performance decreased disproportionately under the
higher-load condition. Adapted with permission from Asloun
et al. (2008).
Author's personal copy
95
% correct responses
120
100
80
60
40
20
Controls
TBI
0
5 10 20
5 10 20
5 10 20
5 10 20
no
interference
motor task
articulatory
suppression
mental
calculation
recall delay (secs)
Fig. 2. Random letter generation. The figure presents an index
of randomness (the Turning Point Index (TPI) which measures
the ability to alternate ascending and descending order in
random generation) according to the generation rate (one
letter every 1, 2, or 4 s). Patients with severe TBI obtained a
significantly lower TPI than controls. Adapted with permission
from Azouvi et al. (1996).
Fig. 3. Short-term memory with interference: Brown–Peterson
task, verbal modality. Subjects were asked to recall three letters
after 5, 10, or 20 s, with or without an interfering task of
increasing complexity. Data are mean (71 SE) percentage
correct responses for the three recall delays and for each
experimental condition. The figure shows the greater proportional decrease of performance of patients with severe TBI, as
compared to controls, when faced with a complex interfering
task. Adapted with permission from Vallat-Azouvi et al. (2007).
subacute/chronic stage after a severe TBI, we
used random number (1–10) generation, at a selfpaced rate to avoid any effect due to slowed
processing (Azouvi et al., 2004; Leclercq et al.,
2000). Compared to controls, patients used a
slower generation rate and obtained a lower score
on a composite index of randomness (Azouvi
et al., 2004; Leclercq et al., 2000).
More recently, we conducted a systematic study
of the three components of working memory.
Thirty patients with severe chronic TBI and 28
controls were assessed (Vallat-Azouvi et al.,
2007). The tasks were designed in order to tap,
as selectively as possible, the main functions of
working memory, according to the Baddeley
model (Baddeley, 1986). Regarding the two slave
systems, a marginally significant impairment was
found in the patient group for digit span (both
forward and backward), while there was no
significant deficit of visual spans. The main group
differences were found with central executive
tasks. The Brown–Peterson paradigm of shortterm memory with interference, described earlier
in this section, was used to assess the ability to
simultaneously store and process information,
both in verbal and visual modalities. Results
showed a dramatic decrease of performance of
patients with TBI under interference. In the
verbal Brown–Peterson task, three interfering
tasks of increasing complexity were used. A
significant triple group by interfering task by
recall delay interaction was found, due to a poorer
performance of TBI patients under the more
demanding interfering task, and for longer recall
delays (Fig. 3). Other central executive tasks,
requiring either simultaneous storage and processing of information, or the ability to update and
monitor information in short-term memory, were
also performed significantly poorer by patients as
compared to controls.
In summary, the results of the different studies
reviewed above suggest that the slave systems of
working memory, responsible for passive storage
of verbal or visual information, are relatively well
preserved after a severe TBI. However, central
executive aspects of working memory (particularly the ability to simultaneously store and
process complex information, or to monitor and
update information) seem to be impaired. This
could be due to impaired activation of executive
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96
networks, as suggested by recent functional neuroimaging studies (Cazalis et al., 2006; Christodoulou
et al., 2001; Fontaine et al., 1999; McAllister et al.,
1999, 2001; Perlstein et al., 2004). Another
important aspect of working memory functioning,
dual-task processing, will be addressed in the
section on divided attention.
Speed of processing and attention
Theoretical aspects
Van Zomeren and Brouwer (1994) proposed a
clinically-oriented model of attention, based on
the assumption that attention can be divided into
four cognitive modules under two broad dimensions, intensity and selectivity, both under the
supervision of an attentional executive supervisory system. Intensity refers to the quantitative
variations in the amount of mental activity
required on a given task. Phasic alertness is the
sudden increase of mental activity, resulting for
example from a warning signal. Sustained attention refers to slower and longer tonic changes of
mental activity, corresponding to the ability to
maintain attention continuously over long periods
of time during which the subject has to detect
and respond to small and/or infrequent changes.
Selectivity refers to the limited amount of
information that can be dealt with, and is in turn
divided into two components: focused and divided
attention. Focused attention refers to the ability to
attend to one particular stimulus, and to discard
irrelevant stimuli (or distractors). Divided attention refers to the ability to share attentional
resources between two simultaneous stimuli.
Behavioral aspects
Attentional disorders are among the most frequent complaints of survivors of a TBI, and of
their close relatives. In a group of 57 severe TBI
patients two years after the injury, 33% complained of mental slowness, 33% of poor concentration, and 21% of inability in doing two things
simultaneously (Van Zomeren and Van den Burg,
1985). Brooks et al. (1986) found that 67% of
relatives reported mental slowness five years postinjury. Difficulty in concentrating was reported by
50% of the relatives seven years after the injury
(Oddy et al., 1985). Therapists using the Rating
Scale of Attentional Behaviour reported that the
most severe problems (out of 14) of severe TBI
patients were: ‘‘performed slowly on mental
tasks,’’ ‘‘been unable to pay attention to more
than one thing at once,’’ ‘‘made mistakes because
he/she wasn’t paying attention properly,’’ and
‘‘missed important details in what he/she is doing’’
(Ponsford and Kinsella, 1991).
Mental slowness
Slowed information processing has been one of
the most robust findings across all neuropsychological studies after TBI (Miller, 1970; Ponsford
and Kinsella, 1992; Van Zomeren, 1981). However, although TBI patients perform slower, they
do not make more errors than controls, at least in
self-paced tasks where they are able to sacrifice
speed to achieve greater accuracy (Ponsford and
Kinsella, 1992). This has been called the speed–
accuracy tradeoff.
Speed of processing was found significantly
inversely correlated with severity of injury
(Van Zomeren and Deelman, 1976), and was one
of the best neuropsychological predictors of
the ability to return to work, seven years after
the injury (Brooks et al., 1987).
Mental slowness is dependent on task complexity and is related to prolonged decision times rather
than to prolonged movement times (Norrman
and Svahn, 1961; Ponsford and Kinsella, 1992;
Van Zomeren, 1981; Van Zomeren and Deelman,
1976). Van Zomeren and Brouwer (1994) carried
out a meta-analysis of seven RT studies in subacute
TBI patients. They found a remarkably constant
ratio (about 1.4) between the RTs of patients and
controls. The ratio appeared slightly larger in more
complex tasks, producing RTs of 700 ms or more in
control subjects.
Phasic alertness
Most neuropsychological studies agree on the fact
that phasic alertness, as assessed by the shortening
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97
of RT when the targets are preceded by a warning
signal, is preserved after TBI (Ponsford and
Kinsella, 1992; Whyte et al., 1997; Zoccolotti
et al., 2000).
Sustained attention
Sustained attention is addressed by measuring the
stability of task performance over relatively long
periods of time. Although the level of vigilance is
reduced in patients with TBI, the existence of a
deficit of sustained attention remains debated.
Most studies found that patients’ performance
did not decrease more than controls’ with time
(Ponsford and Kinsella, 1992; Spikman et al.,
1996; Stuss et al., 1989; Van Zomeren and
Brouwer, 1994; Whyte et al., 2006; Zoccolotti
et al., 2000). But greater variability of performance has been evident in other studies using
continuous tasks requiring an active processing
of a rapid flow of information or the inhibition
of highly automatized responses (Dockree et al.,
2006; McAvinue et al., 2005; Stuss et al., 1989;
Whyte et al., 1995).
Focused attention
Distractibility and difficulty in concentrating are
frequent complaints after TBI, suggesting a
decrease of response selectivity. However, contrary to expectations, a behavioral study in a
naturalistic setting showed that the number and
duration of off-task behaviors of TBI patients
were not particularly influenced by the presence
of distractors (Whyte et al., 1996, 2000). Accordingly, most experimental studies failed to demonstrate disproportionate distraction and sensitivity
to interference. In the Stroop paradigm (Stroop,
1935), subjects are asked to name the ink color of
color names in incongruent conditions, for example, the word ‘‘green’’ written with red ink. Color
naming requires the inhibition of the strong
automatic reading tendency. TBI patients performed the task slower than controls, but without
being more distracted by the interference condition (Chadwick et al., 1981; Ponsford and
Kinsella, 1992; Stuss et al., 1989). Similar negative
findings were found with experimental paradigms
based on response interference, in which distractors strongly elicit response tendencies competing
with those of the target stimuli (Spikman et al.,
1996; Stablum et al., 1994; Van Zomeren and
Brouwer, 1994; Veltman et al., 1996).
However, one study found that distractors
irrelevant to the task (a brightly colored moving
stimulus appearing above the target location),
occurring simultaneously or shortly after the
target, produced slowing of RT that was significantly greater for TBI patients than controls
(Whyte et al., 1998). These data were interpreted
as reflecting a greater distractibility. Also, TBI
participants were found to have more difficulty
than controls to ignore irrelevant information
only in a condition with high target-distractor
similarity (Schmitter-Edgecombe and Kibby,
1998). This suggests that the presence of a deficit
of focused attention may depend on the manner in
which relevant information is made distinct from
irrelevant information.
Divided attention
Clinicians frequently report difficulties in doing
two things simultaneously after TBI. Such difficulties may interfere with daily-life demands, and
with return to work. Divided attention is determined by at least two factors (Van Zomeren and
Brouwer, 1994). The first one is the speed of
processing, and the second corresponds to control
mechanisms involved in sharing resources and
switching between tasks. Divided attention is
closely related to the concept of working memory,
since the ability to carry out two tasks at the same
time is considered as one of the key functions of
the central executive (Baddeley, 1986). However,
the relationships between divided attention and
working memory are complex and debated
(Asloun et al., 2008; Miyake et al., 2000).
Brouwer et al. (1989) and Veltman et al. (1996)
used a dual task combining a visual choice RT and
a driving simulator task in which the difficulty of
each single task was adjusted to the individuals’
performance level. Such adjustment permitted to
control for differences in speed. TBI patients did
not show any disproportionate dual-task decrement as compared with controls (Brouwer et al.,
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98
1989; Veltman et al., 1996). However, a significant
correlation was found within the patient group
between injury severity and divided attention
cost (Brouwer et al., 1989; Veltman et al., 1996).
Indeed, the performance of patients with a PTA
of more than two weeks was poorer, compared
with less severely injured participants. Veltman
et al. (1996) suggested that less severely injured
patients use a compensatory strategy characterized by cautiousness and increased mental effort,
while such strategies would not be available to
more severely injured patients.
Several other studies tended to confirm this
hypothesis and suggested the existence of deficits
of dual-task processing after severe TBI at least in
complex tasks performed under time pressure
(McDowell et al., 1997; Park et al., 1999; Stablum
et al., 1994; Vilkki et al., 1996). McDowell et al.
(1997) used a simple visual RT performed
concurrently with articulation or digit span tasks.
To control for the effect of slowed processing, an
analysis was performed by pairing a subsample
of TBI patients with control subjects matched
for single-task reaction time. The dual-task
decrement assessed in this way was significantly
higher for TBI patients than controls. Park et al.
(1999) reported a meta-analysis on divided
attention after TBI. They found that the effect
size of the divided attention deficit varied
considerably from one study to another (range:
0.03–1.28). TBI patients did not differ from
controls when the divided attention tasks could
be performed relatively automatically, while they
were impaired relative to controls on tasks
including substantial working memory load (Park
et al., 1999).
In our department, we conducted a series of
studies on divided attention that also lead to the
conclusion that deficits were strongly determined
by tasks characteristics. In a first study, severe
subacute TBI patients were given two different
dual tasks (Azouvi et al., 1996). The first task was
performed without time pressure and associated a
modified Stroop paradigm and a random generation task. No disproportionate dual-task impairment was found in the TBI group. The second
task included a higher time pressure. Patients
were asked to perform a card sorting task of
variable difficulty level combined with random
generation of letters at an imposed rate (Baddeley,
1966). A disproportionate decrease in performance occurred under dual-task condition in the
TBI group, even after statistical control for slowed
information processing. These results again suggest that the presence of divided attention deficits
in TBI depends on the attentional demands of
the task, and that in complex resource-demanding
conditions, slowness is not sufficient to explain
such deficit. In two subsequent studies, we used a
dual task combining self-paced random number
generation with a choice visual RT (Azouvi et al.,
2004; Leclercq et al., 2000). Comparatively to
controls, severe TBI patients showed a disproportionate dual-task decrement of performance.
In the second study (Azouvi et al., 2004), two
additional conditions were given, in which subjects were instructed to emphasize alternatively
one of each task. We found that TBI patients
were able to allocate their resources according to
task instructions as efficiently as controls, while
they had difficulties in managing the two tasks
simultaneously (Fig. 4). This suggests that the
divided attention deficit could be related to a
Reaction Time (msec)
1100
1000
Controls
TBI
900
800
700
600
500
400
300
single task
dual task (random generation)
dual task (no emphasis)
dual task (go-no go)
Fig. 4. Dual-task performance. The figure shows the mean
(71 SE) RT of patients and controls in a selective attention
task (go–no go) performed under four conditions: single task,
dual task without any instruction regarding the task to
emphasize, dual task with emphasis on random generation,
and dual task with emphasis on go–no go. Adapted with
permission from Azouvi et al. (2004).
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99
reduction of available central executive resources
rather than to a deficient strategic control
(Leclercq and Azouvi, 2002).
In summary, mental slowness is one of the most
robust findings after severe TBI. Whether attentional functions are additionally impaired remains
debated. The presence of specific impairments of
attentional functions (particularly of divided
attention) may depend on the nature and complexity of the task.
Mental fatigue
Mental fatigue is a highly frequent complaint
after TBI, reported by 30–70% of patients
(Brooks et al., 1986; Dijkers and Bushnik, 2008;
Ponsford et al., 1995a; Ziino and Ponsford, 2005).
Olver et al. (1996) compared patients with
predominantly severe TBI at two and five years
post-injury and found a high prevalence of fatigue
at both time points (respectively 68% and 73%).
Bushnik et al. (2008a, b) found that self-reported
fatigue improved during the first year, and then
did not change significantly up to two years
after TBI. Several studies found no significant
relationships between fatigue and injury severity
(Borgaro et al., 2004; Cantor et al., 2008; Ziino
and Ponsford, 2005). In a population-based study,
five years post-injury, fatigue was reported more
frequently by individuals with severe TBI (58%),
as compared to minor or moderate TBI (35% and
32%), but the difference was not statistically
significant (Masson et al., 1996).
The mechanisms of fatigue after TBI remain
debated. It has been found associated with
depression, pain, disturbed sleep, or neuroendocrine abnormalities (Bushnik et al., 2007; Chaumet
et al., 2008; Clinchot et al., 1998; Kreutzer et al.,
2001). Van Zomeren et al. (1984) argued that
fatigue after TBI could be due to the constant
compensatory effort required to reach an adequate
level of performance in everyday life, despite
cognitive deficits and slowed processing. This is
known as the ‘‘coping hypothesis.’’
The coping hypothesis has received support
from experimental studies. Riese et al. (1999)
assessed the performance of eight very severe TBI
patients in a continuous dual task lasting 50 min.
They found that, although sustained task performance did not significantly differ between TBI
and control subjects, TBI patients showed more
subjective and physiological distress than controls.
They reported higher levels of task load and more
visual complaints. Moreover, while controls’
systolic blood pressure decreased from pre- to
post-test, it showed the reverse pattern in the TBI
group, suggesting higher psychophysiological
costs to sustain task performance. Azouvi et al.
(2004) found that TBI patients, as compared to
controls, reported higher levels of subjective
mental effort during completion of a complex
divided attention task. Ziino and Ponsford
(2006a, b) studied in two parallel studies the
relationships between self-reported fatigue and
cognitive deficits (vigilance and selective attention). In a group of patients with TBI of various
severities, fatigue was significantly correlated
with performance on the vigilance task and on
the complex selective attention test, but not with
more simple attentional tasks.
We assessed the relationships between subjective mental fatigue, mental effort, attention
deficits, and mood in 27 patients with subacute/
chronic severe TBI (Belmont et al., in press).
Subjects first rated their baseline subjective
fatigue on the Fatigue Severity Scale (FSS) and
on the Visual Analog Scale for Fatigue (VAS-F).
Then, they performed a long-duration selective
attention task, separated in two parts. Fatigue on
the VAS-F was assessed again between the two
parts, and at the end of the attention task.
Subjects were also asked to rate on a visual
analog scale the level of subjective mental effort
devoted to the task. Patients reported a higher
baseline fatigue than controls. They performed
significantly poorer on the selective attention
task. Significant correlations were found in the
group with TBI between attention performance,
mental effort, and subjective fatigue. In contrast,
fatigue did not significantly correlate with
mood (depression and anxiety). These findings
suggest that patients with more severe attention
deficits have to produce higher levels of mental
effort to manage a complex task, which may
increase subjective fatigue, in line with the coping
hypothesis.
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Executive functions
Theoretical aspects
Executive functions are the cognitive abilities
involved in programming, regulation, and verification of goal-directed behavior. The model
proposed by Shallice (1988) is one of the most
widely used in clinical neuropsychology. This
model proposes two different control levels.
Automatic overlearned motor programs (or schemata) can be executed without conscious control.
Because some of these schemata may conflict with
each other, the model proposes the intervention
of a semiautomatic processor, or ‘‘contention
scheduler,’’ that gives precedence to one of the
conflicting schemata on the basis of internal or
external contingencies. In certain situations, a
subject might need to override automatic actions
and consciously focus its attention elsewhere. The
model proposes a supervisory system to serve this
function. This system is assumed to have limited
capacity. Its main function is to coordinate and
control information processing, particularly in
novel or complex situations. It is generally agreed
that the functions of the supervisory system
depend on multiple separable control processes
located within the frontal lobes (Shallice and
Burgess, 1996).
Behavioral aspects
Survivors from a traumatic coma frequently show
dramatic personality and behavioral changes.
These changes may be related to lack of control
(disinhibition, impulsivity, irritability, hyperactivity, aggressiveness) or lack of drive (apathy,
reduced initiative, poor motivation).These modifications are frequently associated with lack of
awareness (anosognosia). The prevalence of such
disorders after a severe TBI is high. For example,
Brooks et al. (1986) asked the relatives of 55
severe TBI patients to state whether the brain
injured was ‘‘the same person as before the
accident.’’ Three months after the accident, 49%
of relatives answered that the patient was ‘‘not the
same as before,’’ but this proportion increased to
60% at one year and 74% at five years. Five years
post-injury, the most frequent behavioral changes
reported by the relatives were irritability (64%);
bad temper (64%); tiredness (62%); depression
(57%); rapid mood changes (57%); tension and
anxiety (57%); and threats of violence (54%).
Personality change was associated with a high
subjective burden on the relative. In another
study conducted two years after a severe TBI,
irritability was also one of the most frequent
problem, but lack of initiative was reported in
44% of cases, and socially inappropriate behavior
in 26% of cases (Ponsford et al., 1995a).
TBI patients also demonstrate a loss of communication skills, even when basic language
abilities are preserved (McDonald and Flanagan,
2004). Their conversational discourse is disorganized. Some patients are overtalkative but inefficient, often drifting from topic to topic, and
making tangential and irrelevant comments.
Other patients have impoverished communication, with slow and incomplete responses and
numerous pauses. Patients often fail to follow
social conversational rules.
Objective assessment of behavioral modifications is difficult. The Dysexecutive Questionnaire
(DEX) includes 20 items addressing a range of
problems commonly associated with the dysexecutive syndrome (Burgess et al., 1998; Wilson
et al., 1998). It has been found nearly as sensitive
to brain injury as more formal neuropsychological
tests (Bennett et al., 2005). Wilson et al. (1998)
documented with the DEX the five items that
obtained the highest rankings in a group of 16
severely brain-injured patients in a rehabilitation
department: poor planning, poor self-appraisal,
trouble in decision-making, distractibility, and
apathy. The same five items also obtained the
highest ranking (mean score higher than 2/4) in a
study conducted in our department with the same
scale (Cazalis et al., 2001).
Conceptualization and set-shifting
Sorting tasks require subjects to classify items
(cards, tokens) according to varying sorting
criteria (such as color, shape, number of stimuli,
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etc.) to adapt their responses to cues given by the
examiner, and to shift criteria when required to.
The Wisconsin Card Sorting Test (WCST) is the
most widely sorting test used in clinical neuropsychology. It may show a reduction in number of
sorting criteria found by the subject and, more
importantly, shifting difficulties, defined by perseverative errors. The sensitivity of this test in TBI
subjects has been questioned, and seems to
depend on the version of the test used. A number
of studies found a higher number of perseverative
errors after TBI, at least when using the original,
longer, and more difficult version (Ferland et al.,
1998; Stuss et al., 1985), while a modified, easier
version (Nelson, 1976) seems to be less sensitive,
except at the early stage post-injury (Levin et al.,
1990; Spikman et al., 2000). Interestingly, Stuss
et al. (1985) found that the WCST (original
version) was one of the two neuropsychological
tests that best discriminated from controls a
group of brain-injured subjects with apparent good
recovery, but with persisting complaints. Vilkki
(1992) designed a categorization and sorting test
with tokens of different color, size, and shape. TBI
patients performed poorer on that task as compared to healthy controls or to patients with lesions
of the posterior part of brain of different nature.
Planning
The ‘‘Tower of London’’ task addresses the
planning component of the supervisory system
(Shallice, 1982). The test apparatus consists of
three beads of different colors, on three sticks of
different length in a row. Subjects are presented
with two possible arrangements of the beads, the
starting position and the goal position. They are
asked to reach the goal position with as few moves
as possible, but they are not allowed to move
more than one bead at a time, to leave a bead out,
or to put more beads on a stick than possible. TBI
patients performed the Tower of London as
accurately as controls but more slowly (Cockburn,
1995; Ponsford and Kinsella, 1992; Spikman et al.,
2000; Veltman et al., 1996). However, it seems
that at least some patients, with more severe
injuries, may perform poorly on the Tower of
London (Cicerone and Wood, 1987; Levin et al.,
1994; Veltman et al., 1996). Accordingly, we
found a high interindividual variability in a study
with a modified computerized version of the task
(Cazalis et al., 2006). Four severe TBI patients out
of ten obtained a good performance, within the
upper range of healthy controls, in terms of both
speed and accuracy, while six patients (60%)
demonstrated a very poor performance, far below
the range of controls. This variability in performance was accompanied by variability in brain
activation patterns in fMRI, with good performers
showing a brain activation comparable to that of
controls, while poor performers had a reduced
activation of prefrontal and cingulate areas
(Cazalis et al., 2006). Vilkki (1992) designed
another mental planning task, requiring to learn
a spatial configuration by self-set goals. Patients
with TBI performed poorer than controls or than
patients with posterior surgical lesions of the brain
(Vilkki, 1992). However, opposite results were
found by Spikman et al. (2000) in patients at a
later post-injury stage.
Mental flexibility
The Trail Making Test (Reitan, 1958) requires
patients to alternate between two sets of
responses (letters and numbers). Subjects must
first draw lines to connect consecutively numbered circles on one work sheet (part A) and then
connect the same number of consecutively numbered and lettered circles on another work sheet
by alternating between the two sequences
(part B). Patients with TBI performed the task
slower than controls (Dikmen et al., 1990; Levin
et al., 1990). However, it seems that speed of
processing was not significantly more affected by
the more difficult (B) condition as compared to
the easiest (A) condition, suggesting that patients
had no deficit of mental flexibility, in addition to
slowed processing (Spikman et al., 2000).
Generation of new information
Tasks of verbal or design fluency are of common
use in clinical practice. These tasks require the
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ability to generate in a limited time the maximal
number of items pertaining to a given category
(e.g., animals, words beginning with an F,
designs). Impaired performance in TBI patients
is usually characterized by a low number of items
generated per minute, and in some cases, by a
tendency to use repetitive or stereotyped response
patterns (Levin et al., 1990, 1991). As previously
mentioned, TBI patients also have an impaired
ability to generate random series (Azouvi et al.,
1996, 2004).
Inhibition of dominant responses
The Stroop test is usually used to assess inhibition.
Data obtained with this test have been presented
in the section ‘Focused attention’.
Executive functions in a naturalistic setting
Executive functions are by nature mainly involved
in novel, open-ended, and unstructured situations
that are different from most structured neuropsychological tasks or from routine life in a rehabilitation setting. Patients who seem to behave
appropriately while in a stable, quiet, nondemanding environment may show important difficulties
in adapting to more complex situations (Eslinger
and Damasio, 1985; Shallice and Burgess, 1991).
Shallice and Burgess (1991) reported three cases
of frontally-injured patients who had a nearly
normal performance on standard tests, but were
dramatically impaired in two open-ended tests.
The six-element test required patients to carry out
six simple open-ended tasks in 15 min. They had
to judge how much time to devote to each task so
as to optimize their performance given some
simple rules. The second task, the multiple
errands test, involves scheduling a set of simple
shopping activities in real time in a street.
Script generation is another way to assess
everyday life disorders. Cazalis et al. (2001) asked
severe TBI patients to generate scripts, that is, to
spell out in the proper order the successive actions
that were necessary to reach a given goal. Three
scripts of increasing difficulty were given: a
routine (preparing to go to work in the morning),
a nonroutine (taking a trip to Mexico), and a
novel script (opening a beauty salon). The results
showed that TBI patients, in opposition with
patients with focal prefrontal lesions, were able to
generate proper actions, in the correct order, and
to state which actions were the more important
to reach the goal, just as efficiently as controls.
However, when asked to reorganize actions
belonging to different scripts that were presented
in a mixed array, they were less able than controls
to discriminate actions, and tended to make
sorting errors. This was attributed to a difficulty
in dealing with multiple sources of information,
rather than to a deficient access to script knowledge (Cazalis et al., 2001).
Chevignard et al. (2000, 2008) also used a script
generation task in patients with prefrontal lesions.
Patients were required to generate the actions
necessary to prepare two simple meals. Then, in
a second time, they were asked to perform the
task in a real kitchen. In comparison to controls,
patients produced a disproportionate number of
errors in the execution compared to the generation condition.
In the route finding task, patients are required
to reach a previously unknown location in the
hospital (Boyd and Sautter, 1993). Using this task
in a sample of patients with severe TBI, we found
that patients performed poorer than controls
(Cazalis et al., 2001). While they were able to
understand task instructions like controls, they
were less able than controls to set an appropriate
search strategy, to detect and correct errors, and
to memorize information. They also showed more
inappropriate on-task behavior and needed more
prompting from the examiner than controls.
Spikman et al. (2000) found that the route finding
test significantly discriminated patients with
chronic TBI from healthy controls, while all the
other executive tests in this study did not.
Heterogeneity of executive disorders after TBI
Executive functions are not a unitary construct.
Inter-test correlations of measures of executive
functions within a group of 90 patients with TBI
have been found to be weak, and not stronger
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than correlations with nonexecutive tests (Duncan
et al., 1997). A factorial analysis has been conducted on a battery of tests of executive functions
in a sample of 104 TBI patients (Busch et al.,
2005). The results revealed three weakly intercorrelated factors: higher-level executive functions (self-generated behavior and flexibility/
shifting); mental control on information in working memory; and intrusions or perseverations in
long-term memory.
awareness and injury severity is debated.
Prigatano & Altman (1990) did not find any
significant correlation with injury severity, while
Leathem et al. (1998) found that only severe TBI
patients overestimated their skills, in contrast with
individuals with mild and moderate TBI whose
judgment did not differ from that of relatives.
Conclusion
Anosognosia and Lack of Insight
Severe TBI patients have repeatedly been found
to underestimate their difficulties in comparison
to relatives’ and/or therapists’ reports (Prigatano
and Altman, 1990). This lack of awareness mainly
concerns cognitive and behavioral problems,
whereas physical or sensory impairments are
usually acknowledged. Oddy et al. (1985) found
that 40% of TBI patients did not admit memory
difficulties that were reported by family members
seven years post-injury. Sunderland et al. (1983)
found that self-assessment of memory was poorly
correlated with actual memory tests by TBI
patients, in contrast with relatives’ judgment. It
was also found that 33% of severe TBI patients
reported that memory was not a problem at all in
their everyday life, an amount that was similar to
that of patients with mild TBI. Patients with TBI
also underestimate their behavioral modifications,
and overestimate their social skills and emotional
control, in comparison with their relatives’
reports (Fordyce and Roueche, 1986; Prigatano
and Altman, 1990; Prigatano et al., 1990). Lack
of insight is a complex phenomenon and may
reflect (organic) anosognosia and/or psychological
adjustment to neurological impairments (i.e.,
denial). The relationship between lack of
Cognitive deficits after a traumatic coma are
complex, and often difficult to detect and to
measure. Some patients may perform well on
standardized cognitive tests, while showing significant difficulties in everyday life. Moreover,
patients frequently have poor awareness of their
difficulties. For these reasons, assessment of
cognitive deficits should rely on careful examination, including specific psychometric tests, but also
questionnaires for family members, and ecological
measures, in situations close to real life. A
comprehensive assessment and understanding
of cognitive difficulties is important, as there is
now a large agreement on the fact that cognitive
rehabilitation is effective, particularly for deficits
of executive functions, attention and working
memory (Cicerone et al., 2000; Kennedy et al.,
2008).
Acknowledgments
Studies reported in this review were supported by
grants from the French Ministry of Health (PHRC
national 2001, P011204), by AP-HP, by the
Institut Garches and by the Fondation de l’Avenir
pour la Recherche Médicale.
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Appendix
Table A1. Summary of studies of cognitive testing after TBI
Cognitive domain/functions
Long-term memory
Anterograde episodic memory
Learning rate
Semantic encoding
Benefit from semantic memory
aids
Ability to use mental imagery to
improve encoding efficiency
Forgetting rate
Sensitivity to interference
Retrograde memory:
autobiographical memory,
public events, semantic
knowledge
Prospective memory
Implicit and procedural memory
Working memory
Short-term storage
Storage and processing of
information in short-term
memory
Attention
Speed of processing
Phasic alertness
Sustained attention
Focused attention
Divided attention
Executive functions
Conceptualization and set
shifting
Planning
Mental flexibility
Generation of new information
Inhibition of dominant
responses
Executive functions in
naturalistic settings
Testing procedure
Performance (vs. controls)
Verbal/visual learning of new information
Multiple repeated trials of information
presentation
Influence of the relative importance of the
information; spontaneous use of semantic
clustering
Comparison of free recall vs. cued recall
Impaired (below 1 SD/norms)
Slower, inconsistent, and
disorganized learning
Impaired
Comparison of concrete vs. abstract words;
benefit from imagery instructions
Comparison of delayed vs. early recall
Presentation of two successive lists of words
(A and B)
Questionnaires on different personal life
periods; general knowledge
Remembering to perform a previously planned
action, either time-based (performance of
action at a given time point) or event-based
(after a predetermined event has occurred)
Priming effect; skill learning
Preserved
Impaired
Accelerated forgetting rate
Impaired retroactive interference
(effect of list B on list A) but
preserved proactive
interference
Impaired without temporal
gradient
Impaired
Debated (seems preserved only
for automatic tasks)
Digit or visual spans
PASAT; n-back; updating and monitoring;
Brown–Peterson (interference in
short-term memory)
Mildly impaired
Load-dependant impairment
Timed tasks (reaction times, PASAT, etc.)
Benefit from a warning signal
Stability of performance over a long period of
time
Ability to discard irrelevant stimuli or distractors
(e.g., Stroop test)
Dual tasks
Reduced
Preserved
Debated seems relatively
preserved
Preserved
Sorting tasks
Tower of London or other planning tasks
Trail Making Test
Verbal or design fluency; Random generation
Stroop test
Open-ended tasks (multiple errands;
six-element; route finding; kitchen task)
Load-dependant impairment
Impaired (at least with more
difficult versions of the task)
Debated, seems relatively
preserved
Preserved (but slowed)
Impaired
Preserved
Impaired
Note: For clarity of presentation, references for tasks and studies are not included in the table, but they are indicated in the text.
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