revue neurologique 173 (2017) 461–472

Available online at

ScienceDirect
www.sciencedirect.com

Neuropsychology

Neuropsychology of traumatic brain injury: An

expert overview

P. Azouvi a,*,b, A. Arnould a,b, E. Dromer a,b, C. Vallat-Azouvi b,c,d

a
Service de médecine physique et de réadaptation, hôpital Raymond-Poincaré, AP–HP, 104, boulevard
Raymond-Poincaré, 92380 Garches, France
b
HANDIReSP EA 4047, université de Versailles Saint-Quentin, 78423 Montigny-Le-Bretonneux, France
c
Laboratoire de psychopathologie et neuropsychologie, EA 2027, université Paris-8-Saint-Denis, 2, rue de la Liberté,
93526 Saint-Denis, France
d
Antenne UEROS- UGECAMIDF, hôpital Raymond-Poincaré, 104, boulevard Raymond-Poincaré, 92380 Garches,
France

info article abstract

Article history: Traumatic brain injury (TBI) is a serious healthcare problem, and this report is a selective
Received 6 March 2017 review of recent findings on the epidemiology, pathophysiology and neuropsychological
Accepted 13 July 2017 impairments following TBI. Patients who survive moderate-to-severe TBI frequently suffer
Available online 26 August 2017 from a wide range of cognitive deficits and behavioral changes due to diffuse axonal injury.
These deficits include slowed information-processing and impaired long-term memory,
Keywords: attention, working memory, executive function, social cognition and self-awareness. Men-
Traumatic brain injury: Cognition tal fatigue is frequently also associated and can exacerbate the consequences of neuropsy-
Executive function chological deficits. Personality and behavioral changes can include combinations of
Memory impulsivity and apathy. Even mild TBI raises specific problems: while most patients recover
within a few weeks or months, a minority of patients may suffer from long-lasting
symptoms (post-concussion syndrome). The pathophysiology of such persistent problems
remains a subject of debate, but seems to be due to both injury-related and non-injury-
related factors.
# 2017 Elsevier Masson SAS. All rights reserved.

Traumatic brain injury (TBI) has been defined as ‘‘an alteration
in brain function or other evidence of brain pathology caused
by an external force’’ [1]. It represents a major health problem,
and is a leading cause of death and disability throughout the
world. Individuals who survive TBI may suffer lifelong
disability, mostly due to cognitive disorders and behavioral
and personality changes. In one prospective longitudinal
study of an inception cohort [2,3], at 4 years after severe TBI
and out of 147 patients, 46 (32%) presented with severe
disability, 58 (40%) with moderate disability and 40 (28%) with
good recovery, according to the Glasgow Outcome Scale.
Overall, although 79% were independent in terms of simple
daily living activities, 40–50% needed help for outdoor or
organizational activities. Only a minority (36%) declared having
any professional activity.
The present review summarizes recent research regarding
epidemiological and neuroimaging findings in patients with
TBI, and also focuses on the main cognitive and behavioral

* Corresponding author.
E-mail address: Philippe.azouvi@aphp.fr (P. Azouvi).
http://dx.doi.org/10.1016/j.neurol.2017.07.006
0035-3787/# 2017 Elsevier Masson SAS. All rights reserved.
462 revue neurologique 173 (2017) 461–472
impairments that may arise in patients with moderate-to-
severe TBI. The issue of mild TBI, which raises its own specific
questions, is also briefly addressed.
1. Epidemiology of TBI
The main causes of TBI are road traffic accidents, falls, assault
and sports-related injuries. Typically, TBI predominantly
affects young adult males (aged 15–25 years) after road traffic
accidents. However, two other peak incidences are found in
young infants and in elderly people, particularly after falls [4].
Roozenbeek et al. [5] recently outlined the changing epide-
miological pattern of TBI. They claimed that the median age of
patients with TBI is increasing and that falls (which pre-
dominantly affect older individuals) are now the leading cause
of TBI, overtaking road traffic accidents. In a recent review,
Brazinova et al. [6] found wide variability across countries and
regions for crude incidence rates of TBI (47.3–849 per 100,000
population per year), mean age at injury (range: 26.7–44.5
years) and gender ratio, although all studies reported greater
incidences in males (range: 55–80%). Also, lower socioecono-
mic status, preexisting psychiatric disorders and/or substance
abuse have repeatedly been significantly associated with
higher risks of sustaining TBI [7].
2. Severity of TBI
This factor is measured by the Glasgow Coma Scale (GCS) [8] or
by duration of post-traumatic amnesia (PTA). According to the
GCS, severe TBI corresponds to a score of 3–8, moderate TBI to
a score of 9–12 and mild TBI to a score of 13–15 [9]. However,
PTA duration has proved to be a stronger predictor of outcome
than the GCS [10,11]. In earlier classifications, TBI was defined
as mild if the duration of PTA was < 1 h, moderate if between
1–24 h and severe if between 1–7 days [12], whereas more
recent classifications consider that mild TBI may be associated
with PTA for up to 24 h [13]. In any case, approximately 70–90%
of TBI cases are considered mild, while 10–20% of cases are
moderate to severe [4].
3. Functional neuroanatomy of TBI
TBI results in a combination of both focal and diffuse primary
injuries, with secondary damage due to systemic complica-
tions. Primary brain injury includes contusions, which mostly
involve basal and polar regions of the frontal and temporal
lobes due to impact against skull protuberances, and diffuse
axonal injury (DAI) [14,15]. DAI is due to shear strain caused by
acceleration/deceleration forces that ultimately lead to dis-
connection and Wallerian degeneration. Secondary injuries
are related to ischemia, brain swelling and other complex
mechanisms such as inflammation, and may in themselves
have severe consequences [16].
While traditional neuroimaging techniques such as
computed tomography (CT) and magnetic resonance imaging
(MRI) are very useful for identification of life-threatening
intracranial injury at the acute stage, they are not sensitive
enough for DAI, and remain poorly correlated with functional
outcome and cognitive impairment [17]. However, recent
advances in neuroimaging have led to a better understanding
of the functional neuroanatomy of cognitive disorders
associated with TBI [18,19]. The use of positron emission
tomography (PET) in patients with severe TBI, but no detectable
macroscopic structural lesions, revealed that cognitive dis-
orders are significantly related to decreased glucose metabo-
lism at rest in prefrontal and cingulate areas [20].
Diffusion tensor imaging (DTI) is a much more widely
available technique that permits detailed analyses of altera-
tions in white-matter pathway microstructure. Hulkower et al.
[21] showed that DTI is able to differentiate patients with TBI
from controls even after mild TBI and regardless of the time
interval since injury. Moreover, many studies have found
significant relationships between DTI measures and outcomes
[22]. Abnormal DTI measures have been found in the corpus
callosum, cingulum bundle, corona radiata and internal capsule
[21,23]. A few studies reported significant relationships between
DTI measures and cognitive outcomes [24,25], whereas func-
tional MRI (fMRI) has been used to assess changes in brain
activation while performing cognitive tasks. For example,
Perlstein et al. [26] found that deficits of working memory in
patients with moderate-to-severe TBI were related to altered
patterns of activation in working-memory-related brain
regions, including the dorsolateral prefrontal cortex and Broca’s
area. Turner and Levine [27] found that, despite equivalent task
performance on an executive working-memory task, patients
with TBI exhibited augmented functional recruitment in the
prefrontal cortex and posterior regions. Recent studies based on
resting-state fMRI found that TBI was associated with reduced
connectivity in brain networks involved in attentional and
executive functions [28–34]. In particular, alterations in the
default mode network (DMN) appear to be a robust finding in
the literature. The DMN is activated ‘at rest’ and shows reduced
activation (deactivation) during attention-demanding tasks.
Although there have been contradictory findings, modifications
of functional connectivity within the DMN or between the DMN
and other brain networks have been found post-TBI, and may
be linked to cognitive deficits [30,35].
4. TBI and long-term memory
After emerging from coma, patients usually pass through a
phase of global cognitive disturbance generally termed ‘post-
traumatic amnesia’ (PTA) [12]. At this stage, patients are
confused, disoriented in time and place, and unable to store or
retrieve new information; some degree of retrograde amnesia
is usually present as well. Recovery is usually gradual, and a
consistent return of continuous memory indicates PTA
clearing. However, impaired memory frequently persists
afterwards. Problems with memory are the most frequent
subjective complaints reported by TBI patients and their
relatives [2,36,37]. In a recent prospective inception cohort
study of 147 patients, Jourdan et al. [2] found, at 4 years post-
injury, that memory failures were the most frequent
complaints, reported by 67.5% of patients.
Anterograde long-term episodic memory has been among
the most extensively studied domains [38]. Patients with
 revue neurologique 173 (2017) 461–472
severe TBI have poorer performances than controls in all types
of verbal or visual memory tasks [39]. Zec et al. [40] found that
the mean index scores for the Wechsler Memory Scale–
Revised were < 1 SD of the norms for all long-term memory
indices at an average of 10 years post-injury. However, the
mechanisms underlying episodic memory deficits are still a
matter of debate. Compared with healthy controls, patients
with TBI have slower learning rates and accelerated forgetting
rates, inconsistent and disorganized learning, a reduced
ability to spontaneously use active or effortful semantic
encoding, or visual imagery to improve encoding efficiency,
and a greater vulnerability to retroactive interference [40–44].
Yet, they are able to benefit from memory aids such as
semantic cues or recognition [43]. Vanderploeg et al. [45]
evaluated the recovery of verbal memory processes up to 1
year post-injury and found evidence of impaired consolidation
mechanisms, as reflected by relatively more rapid forgetting,
underlying memory impairment. Chiou et al. [46] compared
two groups of patients, one with and one without learning
deficits, and found, using logistic regression, that working-
memory capacity was the most significant predictor of
learning ability after TBI.
Retrograde amnesia has been less extensively studied. A
high prevalence of retrograde memory deficit has been reported
after TBI, encompassing the domains of both autobiographical
memories and memories of public events as well as early
acquired basic and cultural knowledge [47]. Piolino et al. [48]
found that the ability to recall autobiographical episodes and
spatiotemporal details is impaired in patients with chronic
(lasting > 1 year) TBI and has no temporal gradient. Interestin-
gly, deficits involved not only the ability to recall memories, but
also the ability to mentally travel back through subjective time
to re-experience the past (‘autonoetic consciousness’) and to
perceive oneself as a continuous entity across time (self-
perspective). These disorders were significantly correlated with
tests of executive function [48]. More recent studies by the same
group [49,50] found that patients with TBI were impaired
compared with controls in the retrieval of both semantic and
episodic retrograde autobiographical memories, and a large
proportion of their deficits, particularly regarding retrieval of
lifetime periods, general events and specific events, was
mediated by executive deficits. Recent findings now suggest
that deficits in ability to remember the personal past are
associated with a reduced ability to imagine possible events in
the personal future [50,51].
While little research has been carried out on prospective
memory following TBI, all such studies found evidence of
deficits in both time- and event-based prospective memory
[52] that were related to impaired executive functions [53].
Mioni et al. [54] assessed time-based prospective memory after
TBI, and found that patients monitored themselves more
often, but less accurately, than did healthy controls at the
target time, and their performances were related to executive
functions.
5. TBI and working memory
Only a few studies have systematically addressed the various
subcomponents of working memory in survivors of severe TBI.
463
The n-back task offers an opportunity to assess the effects of
parametric increases in working-memory load with no other
changes in task structure. In the task, subjects are presented at
a string of stimuli (letters, digits, figures. . .) at a regular rate
and are required to decide whether the current stimulus
matches something from n steps earlier in the series. Perlstein
et al. [26] found that patients with either moderate or severe
TBI were impaired in terms of performance accuracy, but not
in speed of responding, except for the more demanding 2- and
3-back conditions. Asloun et al. [55] found a load-dependent
deficit with a decrease in accuracy (% hits) in the 2-back
condition in patients with severe TBI.
Random generation has been used in a series of studies to
assess central executive aspects of working memory. This
requires patients to spell out a sequence of items (letters or
numbers) as close as possible to a random series, an ability
shown to depend on a limited-capacity response-selection
mechanism similar to the central executive system. It was
found that, compared with controls, the ability to generate
random series was impaired in patients with severe TBI and
that patients’ randomness indices deteriorated with the
increasing rate of random generation [56–58].
Vallat-Azouvi et al. [59] conducted a systematic study of
different components of working memory in patients with
severe chronic TBI, and found only marginally significant
impairment on forward and backward digit-span tasks. The
main group differences were found with central executive
tasks, such as the Brown-Peterson paradigm of short-term
memory with interference, which requires the ability to
simultaneously store and process information in both verbal
and visual modalities.
Dobryakova et al. [60] used a novel paradigm, CapMan, to
dissociate the capacity and manipulation subprocesses of
working memory. They found that healthy control partici-
pants performed significantly better than TBI participants
when manipulation demands were high, whereas there was
no significant group difference when capacity demands were
high. This finding suggests that TBI mainly impairs the ability
to manipulate information within working memory rather
than working-memory capacity itself.
Dunning et al. [61] recently performed a meta-analysis
including 21 selected studies of working-memory impairment
in survivors of moderate-to-severe TBI. Results showed that
those with TBI had significant deficits in verbal short-term
memory and in both visuospatial and verbal working memory.
Effect sizes ranged from 0.37 to 0.69.
6. TBI, speed of processing and attention
Mental slowness and attentional disorders are, after memory
failure, among the most frequent complaints in TBI survivors
and their close relatives. Jourdan et al. [2] found that such
problems ranked among the five most frequent subjective
complaints reported by patients at 4 years post-injury: mental
slowness and concentration difficulties were reported by
56.7% of patients, and dual-task difficulties by 51.7%.
Slower information-processing is also among the more
robust findings across all post-TBI neuropsychological studies
[62,63]. Mental slowness is significantly correlated with injury
464 revue neurologique 173 (2017) 461–472
severity and task complexity [62,63]. However, a number of
studies have reported that, while patients performed slower
than controls, they did not make more errors, at least in self-
paced tasks where they were able to sacrifice speed to achieve
greater accuracy (speed–accuracy trade-off) [64].
Attention is a multidimensional concept that, according to
van Zomeren and Brouwer [65], can be subdivided into various
modules, such as phasic alertness, sustained attention,
focused attention and divided attention. Most neuropsycho-
logical studies agree that phasic alertness, as assessed by
shortened reaction times when targets are preceded by a
warning signal, is preserved after TBI [62,66]. In contrast, a
deficit in sustained attention, as assessed by measuring the
stability of task performance over relatively long periods of
time, is still being debated. Indeed, most studies found that
patients’ performances did not decrease more than did the
controls’ over time [62,67,68], although a few contradictory
results have suggested greater variability in performance of
continuous tasks requiring active processing of a rapid flow of
information or inhibition of highly automatized responses
[66,69–71].
As for focused attention, most experimental studies have
failed to demonstrate any disproportionate distraction and
sensitivity to interference beyond slower processing speed
when using the Stroop task [62] or other experimental
paradigms based on response interference [67,72]. A meta-
analysis by Ben David et al. [73] showed that, while Stroop
interference was significantly greater in TBI groups compared
with controls, the effect was strongly biased by mental
slowness and changes in sensory processing. Similar findings
have also been reported with selective-attention tasks
requiring participants to selectively pay attention to presented
stimuli and to respond according to a set of rules [74–76], with
processing speed accountng for a significant part of the
impaired performance.
Difficulties in dealing with two tasks at the same time is a
frequent complaint of patients with TBI, and is also frequently
reported by patients’ relatives and clinicians [2,36,77]. There
has been controversy in the literature as to whether divided
attention deficits are related only to slowed information-
processing or to additional impairments of executive control
(task switching, strategic allocation of resources. . .). A number
of studies have found that, when slower processing was
controlled for either experimentally or statistically, there was
no residual impairment of divided attention [62,67,72,78,79].
However, mixed results have been reported, thereby suggest-
ing a deficit of dual-task processing after severe TBI even after
adjusting for slowed processing, at least in complex tasks
performed under time constraints [56–58,80]. These appa-
rently contradictory findings may be related to the nature of
the task [81], as TBI patients did not differ from controls when
divided attention tasks could be performed relatively auto-
matically, whereas they were impaired in tasks involving a
substantial working-memory load [81].
In summary, mental slowness is one of the most robust
findings following severe TBI and may account for a large part
of attentional impairment [75,76]. The presence of specific
impairment of attentional function (particularly divided
attention) beyond slowed processing may depend on the
nature and complexity of the task [82].
7. TBI and mental fatigue
Mental fatigue is a very frequent complaint post-TBI, reported
by 30–70% of patients [83–86]. The presence of fatigue was
reported by 53.3% of a sample of 147 patients followed for 4
years after severe TBI [2]. Bushnik et al. [84] found that self-
reported fatigue improved during the first year of TBI and then
did not change significantly for up to 2 years afterwards.
The mechanism(s) of fatigue after TBI continue to be
debated. It has been associated with depression, pain,
disturbed sleep and neuroendocrine abnormalities [83,86].
Van Zomeren et al. [87] argued that fatigue after TBI could be
due to the constant compensatory effort required to reach
adequate levels of performance in everyday life in the face of
cognitive deficits and slower processing, known as the ‘coping
hypothesis’. Similarly, Azouvi et al. [57] found that TBI
patients, compared with controls, reported higher levels of
subjective mental effort while completing a complex task of
divided attention, whereas in line with the coping hypothesis,
a number of studies have found significant relationships
between subjective mental fatigue and performance of tasks
of selective attention or vigilance [74,88–90]. However, an
inverse relationship is also possible, as Sinclair et al. [70] noted
that self-reported fatigue has a global impact on attentional
performance.
8. TBI and executive function
Given the vulnerability of the frontal lobes and anterior brain
networks to TBI, it is not surprising that patients surviving
severe TBI frequently exhibit executive-function deficits [91].
Loss of conceptualization and set-shifting ability have been
found using sorting tasks like the Wisconsin Card Sorting Test
(WCST) [92], which requires the ability to sort items according
to a given category, then to modify the sorting criteria when
the rule changes. A number of studies have found a larger
number of perseverative errors after TBI, at least when using
the original, longer and more difficult version of the WCST [93],
whereas a modified, easier version [94] appears to be less
sensitive except during early stages post-injury [79] or in older
patients [95].
Planning has also been frequently studied using the
Tower of London [96]. This task requires the subject to
rearrange the colored beads on three vertical rods to match a
model using as few moves as possible. TBI patients
performed this task as accurately as did the controls, albeit
more slowly [62,79].
Mental flexibility is usually assessed by the Trail-Making
Test [97], which requires patients to draw lines to connect
consecutively numbered circles on one worksheet (part A),
and then to alternate between letters and numbers in another
(part B). A number of studies have found that, although
patients with TBI performed the task slower than controls,
they were not significantly more affected by the more difficult
(part B) condition compared with the easier (part A) condition,
suggesting no deficit of mental flexibility in addition to slowed
processing [72,79,98–101], although divergent results were
reported by Periáñez et al. [102].
 revue neurologique 173 (2017) 461–472
The generation of new information is assessed through
tasks of verbal or design fluency that require an ability to
generate, within a limited time, as many items pertaining to a
given category (such as animals, or words beginning with ‘F’).
Patients with TBI usually generate fewer items per minute
and, in some cases, may even show a tendency to use
repetitive or stereotyped response patterns [95,103,104].
However, Draper and Ponsford [101] surprisingly found that
the test did not significantly differentiate TBI patients from
controls at 10 years post-injury.
Inhibition is a concept closely related to selective attention
and working memory. It may be assessed by the Stroop test
[105], in which subjects are asked to name the ink color of color
names under non-congruent conditions. Color-naming requi-
res inhibition of the strong automatic reading tendency.
Earlier studies found that TBI patients performed this task
slower than controls, but were no more distracted by the
interfering condition [62,67], whereas more recent studies
have reported significant effects of interference [106–108].
Other tasks requiring the ability to inhibit a strongly activated
response that is no longer relevant have also proved sensitive
to TBI [101,109].
In fact, the sensitivity of traditional tests of executive
function has been questioned. Some patients who perform
within normal limits on paper-and-pencil tests may yet
show difficulties in adapting to complex situations of daily
life [110]. Such dissociation raises concerns as to the
ecological validity of neuropsychological testing of executive
functions. To address this issue, several researchers pro-
posed using tasks that are more similar in structure to the
open-ended situations encountered in daily life, such as
going shopping, finding one’s way in natural surroundings,
preparing a meal and dealing with a complex multitasking
situation. Such tasks include the Multiple Errands Test [110],
Six Elements Test [110], Executive Function Route-Finding
Task [111,112], ecological cooking test [113,114] and
Executive Secretarial Task [79,115]. Another approach relies
on questionnaires, which may be completed by either the
patient, or a close relative or therapist. The Dysexecutive
Questionnaire (DEX) comprises 20 questions, addressing a
range of problems commonly associated with dysexecutive
syndrome [116], which have proved to be nearly as
sensitive to brain injury as more formal neuropsychological
tests [117]. In a longitudinal study of patients with severe TBI,
it was found that, 4 years post-injury, the DEX was
significantly related to cognitive and mood disorders, and
also the ability to independently carry out elementary and
extended activities of daily living and to return to work,
thereby suggesting good ecological validity. Recently, Azouvi
et al. [118] directly compared, in patients with TBI, the
sensitivity of traditional tests of executive function with a
new questionnaire, the Behavioural Dysexecutive Syndrome
Inventory. Of the 54 patients for whom both behavioral and
cognitive assessments were available, executive function
deficits were found in 87%, of whom 49% had combined
behavioral and cognitive disorders, 6.4% a pure cognitive
impairment and 45% a pure behavioral disorder. This
suggested normal cognition in contrast to the behavioral
modifications in everyday life reported by the closest
relatives.
465
9. Social cognition and TBI
Social cognition is a complex construct referring to the ability
to understand the behavior of others and to react accordingly
in social situations. (A detailed review of social cognition and
TBI is presented in another part in this special issue.) Briefly,
recent studies have shown that patients with TBI are impaired
in various aspects of social cognition, including emotion
perception, assessed by the ability to recognize socially
relevant information (facial expressions of emotion); unders-
tanding the internal state of other people (Theory of Mind);
and empathy (for a review, see McDonald [119]). Nevertheless,
the relationships between impaired social cognition and more
global cognitive deficits are still under debate. Spikman et al.
[120] found no significant correlations between social and non-
social cognition tests, and concluded that poor performances
on social cognition tests were not due to general cognitive
deficits. In a parallel study, the same researchers reported that
impaired recognition of sadness and anger was significantly
correlated with behavioral problems and impaired self-
awareness [121]. In contrast, Milders et al. [122] found no
significant correlation between impaired social cognition and
severity of behavioral problems.
10. Lack of awareness (anosognosia) and TBI
Lack of awareness of cognitive and behavioral disorders has
frequently been reported in TBI patients, especially after
severe TBI [123–126]. Lack of awareness is significantly related
to poorer outcomes [127,128], probably due to less patient
engagement in the rehabilitation program. There is, however,
no consensus on how to measure anosognosia. Sherer et al.
[129] showed that, according to the assessment method, the
frequency of patients with poor awareness varied from 76% to
97%. Moreover, there may be different types of awareness, as
suggested by Ownsworth et al. [130] who, using hierarchical
cluster analysis, distinguished four types of awareness: poor
self-awareness; high defensiveness; high symptom-reporting;
and good self-awareness. The poor self-awareness and high
symptom-reporting typologies had poorer outcomes than the
other two.
The relationship between lack of awareness and executive
function deficits has also been a matter of debate. Bogod et al.
[131] found a significant and positive correlation between
anosognosia and deficits of inhibition and mental flexibility.
Likewise, Ciurli et al. [132] found that patients with poor self-
awareness had more problems with some components of the
executive system. Significant relationships have also been
found between lack of awareness and the ability to take into
account the mental state of another person and to detect false
beliefs [133], and the ability to recognize facial expressions of
anger and fear [121]. Other studies have suggested that lack of
awareness could be related to difficulties in error monitoring
[125]. Bivona et al. [134] found that a lack of self-awareness was
significantly related to difficulty in assuming someone else’s
perspective. Morton and Barker [135] showed, using hierar-
chical regression, that severity of injury, intelligence quotient
(IQ), mood state, and executive and implicit functions all made
466 revue neurologique 173 (2017) 461–472
significant, unique contributions to selective aspects of
awareness. These results suggest that lack of awareness after
TBI is a complex, multidimensional issue.
11. Behavioral changes
Survivors of severe TBI frequently show dramatic personality
and behavioral changes, which can have major consequences
on family, social and vocational reintegration, and on quality
of life [136,137]. Such changes may be related to lack of control
(disinhibition, impulsivity, irritability, aggressiveness) or lack
of drive (apathy, reduced initiative, poor motivation). In a
study conducted 2 years after severe TBI, irritability was one of
the most frequent problems (67%), with lack of initiative
reported in 44% of cases and socially inappropriate behavior in
26% [138]. Recently, Ciurli et al. [139] assessed 120 patients
with severe TBI and found a wide range of neuropsychiatric
symptoms, including apathy (42%), irritability (37%), dyspho-
ria/depressed mood (29%), disinhibition (28%), eating distur-
bances (27%) and agitation (24%). These personality changes
were also associated with a high subjective burden for the
patients’ relatives [140–142].
Recent studies have proposed new multidimensional
approaches to take into account the complexity of the
underlying psychological, cognitive, social, environmental and
personal processes, and the dynamic nature of such problematic
behaviors [143–145]. Using cluster analysis, Arnould et al. [146]
identified four subgroups of patients: (i) those with high scores
for all apathy dimensions (lack of interest, lack of initiative,
emotional blunting); (ii) those with low scores for all dimensions;
(iii) those with isolated major emotional blunting; and (iv) those
with high scores only for lack of initiative and lack of interest.
Rochat et al. [147] used the conceptual framework of
Whiteside and Lynam [148], which identifies four dimensions
of impulsivity:
 urgency (tendency to experience strong reactions often
under conditions of negative affect);
 lack of premeditation (difficulty in thinking and reflecting on
consequences before engaging in an act);
 lack of perseverance (difficulty in remaining focused on a
task that may be boring or difficult);
 sensation-seeking (tendency to enjoy and pursue exciting
activities, and an openness for new experiences).
They found that urgency, lack of premeditation and lack of
perseverance were all increased significantly after TBI,
whereas sensation-seeking decreased significantly, according
to patients’ significant others. In addition, Rochat et al. [145]
found a significant positive correlation between urgency and
deficits of prepotent response inhibition in patients with TBI.
12. Mild TBI
For this complex issue, there is as yet no consensus on how to
define mild TBI; the most widely used definition comes from
the American Congress of Rehabilitation Medicine (ACRM)
Mild Traumatic Brain Injury Committee [149], wherein mild
TBI requires at least one of the following: loss of consciousness
for  30 min; initial GCS score of 13–15 after 30 min; PTA for
 24 h; any altered mental state at the time of accident; and/or
focal neurological deficit(s) that may or may not be transient.
While the majority of cases fully recover within a few weeks or
months, it appears that a significant minority of patients may
experience long-lasting symptoms. Such patients, dubbed the
‘miserable minority’ [150,151], suffer from a range of sub-
jective symptoms, including various combinations of somatic
complaints (headache, dizziness, fatigue. . .), cognitive
complaints (attentional and memory failure), behavioral
modifications (irritability, apathy. . .) and psychological trou-
bles (anxiety, depression, sleep disorders. . .).
The diagnosis of post-concussion syndrome (PCS) requires
the presence of at least three symptoms at either 1 or 3 months
after injury, depending on the classification system used [152].
However, these symptoms are not specific to TBI and may
appear in other conditions, including non-injured patients and
injured patients without TBI [153]. Nevertheless, it appears
that PCS is more frequent following mild TBI than after other
types of injuries, and around 15–20% of patients suffer from
persistent PCS [154–156]. In a recent study of 1716 adults with
mild TBI after motor-vehicle collisions, Hartvigsen et al. [157]
found that, 6 weeks after the accident, 75% reported having
more than three symptoms and 30% had clinically significant
pain. Over time, the prevalence of symptoms and pain
decreased, but were still commonly reported after 1 year.
Dikmen et al. [155] followed 421 patients with mild TBI and
found that these patients reported significantly more symp-
toms than their trauma controls after both 1 month and 1 year,
and about half of them reported three or more post-traumatic
symptoms at 1 year post-injury. McMahon et al. [158], who
reported on findings obtained from 375 mild TBI patients,
found that, at both 6 and 12 months after mild TBI, 82% were
still reporting at least one PCS symptom. Furthermore, 44.5%
and 40.3% of them had significantly lower Satisfaction With
Life Scale scores at 6 and 12 months, respectively, and 22.4% of
those available for follow-up 1 year after injury were still
below full functional status. They concluded that the term
‘mild’ is a misnomer for this patient population.
The mechanisms underlying outcomes after mild TBI
remain a subject of controversy. While abnormal CT findings
are unusual in such patients, recent studies show that more
sophisticated imaging methods, such as DTI or fMRI, can
detect abnormalities in a number of patients, although the
relationships between brain imaging and outcome are still
controversial (for a review, see Sharp and Ham [34]). In fact,
other non-injury-related factors also seem to have a major
influence on outcome, as several studies have shown that
post-traumatic complaints can be influenced by psychological
factors like stress, anxiety, perception of illness, symptom
expectations, litigation and/or premorbid psychiatric condi-
tions [159–161]. Indeed, several recent studies revealed that
post-traumatic stress disorder (PTSD) is frequently associated
with mild TBI, and there is now increasing evidence
suggesting that mild TBI can increase risk for PTSD and that
persistent impairment after mild TBI is largely related to stress
reactions (for a review, see Bryant [162]). In addition, in their
recent systematic review, Silverberg et al. [163] could find no
 revue neurologique 173 (2017) 461–472
multivariable prognostic model that adequately predicts
individual patient outcomes, although the more robust
prognostic factors identified were pre-injury mental health
and early post-injury neuropsychological functioning. Inter-
estingly, compared with these factors, the severity of mild TBI
itself was of little long-term prognostic value. These studies
suggest that outcomes after mild TBI are determined by a
complex interaction of biopsychosocial factors.
Although the presence of neuropsychological deficits has
been well established in the acute stage (within the first 3
months) of mild TBI, most studies could find only marginal,
persistent chronic effects of injury when confounding factors,
such as PTSD, anxiety and litigation, were controlled for
[155,159,164–167]. In a recent large-scale longitudinal study,
Dikmen et al. [155] found that, at 1 year post-injury, except for
an isolated difficulty on a memory test in a subgroup of patients
with GCS scores of 13–14 and abnormal CT scans, no differences
were observed for any neuropsychological measures compared
with trauma controls, despite the persistence of three or more
post-traumatic symptoms in around half the patients.
13. Conclusion
TBI is a complex condition, and patients with moderate-to-
severe TBI are at high risk of having long-lasting cognitive
difficulties and behavioral changes that may impede their
social and vocational recovery, and adversely affect their own
and their families’ quality of life. Thus, TBI patients may need
the long-term support of healthcare professionals, including
cognitive rehabilitation as well as social, vocational and family
support. Indeed, recent findings have suggested that specific
community re-entry services may be useful for preventing long-
term patient deterioration [168]. Mild TBI is also a complex issue
that, despite its apparent initial benignity, may have serious
consequences, especially in people who are more vulnerable.
There is a need to develop services specifically targeted at these
patients to prevent, as far as is possible, persistent PCS.
Role of funding source
Research presented in this paper has been supported by the
French Ministry of Health (Programme Hospitalier de Recher-
che Clinique 2004) grant number AOM04084, and the Institut
de Recherche en Santé Publique (IRESP). It was also supported
by Assistance publique–Hôpitaux de Paris (AP-HP).
Disclosure of interest
The authors declare that they have no competing interest.
references
[1] Menon DK, Schwab K, Wright DW, Maas AI. Position
statement: definition of traumatic brain injury. Arch Phys
Med Rehabil 2010;91:1637–40. http://dx.doi.org/10.1016/
j.apmr.2010.05.017.
467
[2] Jourdan C, Bayen E, Pradat-Diehl P, Ghout I, Darnoux E,
Azerad S, et al. A comprehensive picture of 4-year
outcome of severe brain injuries. Results from the Paris-
TBI study. Ann Phys Rehabil Med 2016;59:100–6. http://
dx.doi.org/10.1016/j.rehab.2015.10.009.
[3] Jourdan C, Bosserelle V, Azerad S, Ghout I, Bayen E,
Aegerter P, et al. Predictive factors for 1-year outcome of a
cohort of patients with severe traumatic brain injury (TBI):
results from the Paris-TBI study. Brain Inj 2013;27:1000–7.
http://dx.doi.org/10.3109/02699052.2013.794971.
[4] Tiret L, Hausherr E, Thicoipe M, Garros B, Maurette P,
Castel JP, et al. The epidemiology of head trauma in
Aquitaine (France) 1986: a community-based study of
hospital admissions and deaths. Int J Epidemiol
1990;19:133–40.
[5] Roozenbeek B, Maas AIR, Menon DK. Changing patterns in
the epidemiology of traumatic brain injury. Nat Rev Neurol
2013;9:231–6. http://dx.doi.org/10.1038/nrneurol.2013.22.
[6] Brazinova A, Rehorcikova V, Taylor MS, Buckova V,
Majdan M, Psota M, et al. Epidemiology of traumatic brain
injury in europe: a living systematic review.
J Neurotrauma 2016. http://dx.doi.org/10.1089/
neu.2015.4126.
[7] Nordström A, Edin BB, Lindström S, Nordström P.
Cognitive function and other risk factors for mild
traumatic brain injury in young men: nationwide cohort
study. BMJ 2013;346:f723.
[8] Teasdale G, Jennett B. Assessment of coma and impaired
consciousness: a practical scale. Lancet 1974;2:81–4.
[9] Jennett B, Teasdale G. Management of head injuries.
Philadelphia: Davis; 1981.
[10] Katz D, Alexander M. Traumatic brain injury: predicting
course of recovery and outcome for patients admitted to
rehabilitation. Arch Neurol 1994;51:661–70.
[11] Ponsford JL, Spitz G, McKenzie D. Using post-traumatic
amnesia to predict outcome after traumatic brain injury. J
Neurotrauma 2016;33:997–1004. http://dx.doi.org/10.1089/
neu.2015.4025.
[12] Russel WR, Smith A. Post traumatic amnesia in closed
head injury. Arch Neurol 1961;5:16–29.
[13] Committee MTBI. Definition of mild traumatic brain
injury. J Head Trauma Rehabil 1993;8:86–7.
[14] Ommaya AK, Genarelli TA. Cerebral concussion and
traumatic unconsciousness: correlation of experimental
and clinical observations on blunt head injuries. Brain
1974;97:633–54.
[15] Hill CS, Coleman MP, Menon DK. Traumatic axonal injury:
mechanisms and translational opportunities. Trends
Neurosci 2016;39:311–24. http://dx.doi.org/10.1016/
j.tins.2016.03.002.
[16] Nortje J, Menon DK. Traumatic brain injury: physiology,
mechanisms, and outcome. Curr Opin Neurol
2004;17:711–8.
[17] Azouvi P. Neuroimaging correlates of cognitive and
functional outcome after traumatic brain injury. Curr Opin
Neurol 2000;13:665–9.
[18] Bigler ED. Traumatic brain injury, neuroimaging, and
neurodegeneration. Front Hum Neurosci 2013;7:395.
http://dx.doi.org/10.3389/fnhum.2013.00395.
[19] Bigler ED, Maxwell WL. Neuroimaging and neuropathology
of TBI. Neuro Rehabil 2011;28:63–74. http://dx.doi.org/
10.3233/NRE-2011-0633.
[20] Fontaine A, Azouvi P, Remy P, Bussel B, Samson Y.
Functional anatomy of neuropsychological deficits after
severe traumatic brain injury. Neurology 1999;53:1963–8.
[21] Hulkower MB, Poliak DB, Rosenbaum SB, Zimmerman ME,
Lipton ML. A decade of DTI in traumatic brain injury: 10
years and 100 articles later. ANJR Am J Neuroradiol
2013;34:2064–74. http://dx.doi.org/10.3174/ajnr.A3395.
468 revue neurologique 173 (2017) 461–472
[22] Zappalà G, Thiebaut de Schotten M, Eslinger PJ. Traumatic
brain injury and the frontal lobes: what can we gain with
diffusion tensor imaging? Cortex 2012;48:156–65. http://
dx.doi.org/10.1016/j.cortex.2011.06.020.
[23] Maller JJ, Thomson RHS, Lewis PM, Rose SE, Pannek K,
Fitzgerald PB. Traumatic brain injury, major depression,
and diffusion tensor imaging: making connections. Brain
Res Rev 2010;64:213–40. http://dx.doi.org/10.1016/
j.brainresrev.2010.04.003.
[24] Kinnunen KM, Greenwood R, Powell JH, Leech R, Hawkins
PC, Bonnelle V, et al. White matter damage and cognitive
impairment after traumatic brain injury. Brain
2011;134:449–63. http://dx.doi.org/10.1093/brain/awq347.
[25] Wilde EA, Newsome MR, Bigler ED, Pertab J, Merkley TL,
Hanten G, et al. Brain imaging correlates of verbal working
memory in children following traumatic brain injury. Int J
Psychophysiol 2011;82:86–96. http://dx.doi.org/10.1016/
j.ijpsycho.2011.04.006.
[26] Perlstein WM, Cole MA, Demery JA, Seignourel PJ, Dixit
NK, Larson MJ, et al. Parametric manipulation of working
memory load in traumatic brain injury: behavioral and
neural correlates. J Int Neuropsychol Soc 2004;10:724–41.
[27] Turner GR, Levine B. Augmented neural activity during
executive control processing following diffuse axonal
injury. Neurology 2008;71:812–8. http://dx.doi.org/10.1212/
01.wnl.0000325640.18235.1c.
[28] Hillary FG, Slocomb J, Hills EC, Fitzpatrick NM, Medaglia
JD, Wang J, et al. Changes in resting connectivity during
recovery from severe traumatic brain injury. Int J
Psychophysiol 2011;82:115–23. http://dx.doi.org/10.1016/
j.ijpsycho.2011.03.011.
[29] Bonnelle V, Ham TE, Leech R, Kinnunen KM, Mehta MA,
Greenwood RJ, et al. Salience network integrity predicts
default mode network function after traumatic brain
injury. Proc Natl Acad Sci U A 2012;109:4690–5. http://
dx.doi.org/10.1073/pnas.1113455109.
[30] Bonnelle V, Leech R, Kinnunen KM, Ham TE, Beckmann
CF, De Boissezon X, et al. Default mode network
connectivity predicts sustained attention deficits after
traumatic brain injury. J Neurosci 2011;31:13442–51. http://
dx.doi.org/10.1523/JNEUROSCI.1163-11.2011.
[31] Ham TE, Sharp DJ. How can investigation of network
function inform rehabilitation after traumatic brain
injury? Curr Opin Neurol 2012;25:662–9. http://dx.doi.org/
10.1097/WCO.0b013e328359488f.
[32] Pandit AS, Expert P, Lambiotte R, Bonnelle V, Leech R,
Turkheimer FE, et al. Traumatic brain injury impairs
small-world topology. Neurology 2013;80:1826–33. http://
dx.doi.org/10.1212/WNL.0b013e3182929f38.
[33] Sharp DJ, Beckmann CF, Greenwood R, Kinnunen KM,
Bonnelle V, De Boissezon X, et al. Default mode network
functional and structural connectivity after traumatic
brain injury. Brain 2011;134:2233–47. http://dx.doi.org/
10.1093/brain/awr175.
[34] Sharp DJ, Ham TE. Investigating white matter injury after
mild traumatic brain injury. Curr Opin Neurol 2011;24:558–
63. http://dx.doi.org/10.1097/WCO.0b013e32834cd523.
[35] Palacios EM, Sala-Llonch R, Junque C, Roig T, Tormos JM,
Bargallo N, et al. Resting-state functional magnetic
resonance imaging activity and connectivity and cognitive
outcome in traumatic brain injury. JAMA Neurol
2013;70:845–51. http://dx.doi.org/10.1001/
jamaneurol.2013.38.
[36] Van Zomeren AH, Van den Burg W. Residual complaints of
patients two years after severe head injury. J Neurol
Neurosurg Psychiatry 1985;48:21–8.
[37] Brooks DN, McKinlay WW. Personality and behavioural
change after severe blunt head injury: a relative’s view.
J Neurol Neurosurg Psychiatry 1983;46:336–44.
[38] Vakil E. The effect of moderate to severe traumatic brain
injury (TBI) on different aspects of memory: a selective
review. J Clin Exp Neuropsychol 2005;27:977–1021.
[39] Carlozzi NE, Grech J, Tulsky DS. Memory functioning in
individuals with traumatic brain injury: an examination of
the Wechsler Memory Scale-Fourth Edition (WMS-IV).
J Clin Exp Neuropsychol 2013;35:906–14. http://dx.doi.org/
10.1080/13803395.2013.833178.
[40] Zec RF, Zellers D, Belman J, Miller J, Matthews J, Femeau-
Belman D, et al. Long-term consequences of severe closed
head injury on episodic memory. J Clin Exp Neuropsychol
2001;23:671–91. http://dx.doi.org/10.1076/
jcen.23.5.671.1247.
[41] Shum DH, Harris D, O’Gorman JG. Effects of severe
traumatic brain injury on visual memory. J Clin Exp
Neuropsychol 2000;22:25–39. http://dx.doi.org/10.1076/
1380-3395(200002)22 [1;1-8;FT025].
[42] Curtiss G, Vanderploeg RD, Spencer J, Salazar AM. Patterns
of verbal learning and memory in traumatic brain injury.
J Int Neuropsychol Soc 2001;7:574–85.
[43] Vanderploeg RD, Crowell TA, Curtiss G. Verbal learning
and memory deficits in traumatic brain injury: encoding,
consolidation, and retrieval. J Clin Exp Neuropsychol
2001;23:185–95.
[44] Crosson B, Novack TA, Trenerry MR, Craig PL. California
Verbal Learning Test (CVLT) performance in severely
head-injured and neurologically normal adult males. J Clin
Exp Neuropsychol 1988;10:754–68.
[45] Vanderploeg RD, Donnell AJ, Belanger HG, Curtiss G.
Consolidation deficits in traumatic brain injury: the core
and residual verbal memory defect. J Clin Exp
Neuropsychol 2014;36:58–73. http://dx.doi.org/10.1080/
13803395.2013.864600.
[46] Chiou KS, Sandry J, Chiaravalloti ND. Cognitive
contributions to differences in learning after moderate to
severe traumatic brain injury. J Clin Exp Neuropsychol
2015;37:1074–85. http://dx.doi.org/10.1080/
13803395.2015.1078293.
[47] Carlesimo GA, Sabbadini M, Bombardi P, Di Porto E,
Loasses A, Caltagirone C. Retrograde memory deficits in
severe closed-head injury patients. Cortex 1998;34:1–23.
[48] Piolino P, Desgranges B, Manning L, North P, Jokic C,
Eustache F. Autobiographical memory, the sense of
recollection and executive functions after severe
traumatic brain injury. Cortex 2007;43:176–95.
[49] Coste C, Agar N, Petitfour E, Quinette P, Guillery-Girard B,
Azouvi P, et al. Exploring the roles of the executive and
short-term feature-binding functions in retrieval of
retrograde autobiographical memories in severe traumatic
brain injury. Cortex 2011;47:771–86. http://dx.doi.org/
10.1016/j.cortex.2010.07.004.
[50] Coste C, Navarro B, Vallat-Azouvi C, Brami M, Azouvi P,
Piolino P. Disruption of temporally extended self-memory
system following traumatic brain injury.
Neuropsychologia 2015;71:133–45. http://dx.doi.org/
10.1016/j.neuropsychologia.2015.03.014.
[51] Rasmussen KW, Berntsen D. Autobiographical memory
and episodic future thinking after moderate to severe
traumatic brain injury. J Neuropsychol 2014;8:34–52.
http://dx.doi.org/10.1111/jnp.12003.
[52] Groot YC, Wilson BA, Evans J, Watson P. Prospective
memory functioning in people with and without brain
injury. J Int Neuropsychol Soc 2002;8:645–54.
[53] Kliegel M, Eschen A, Thone-Otto AI. Planning and
realization of complex intentions in traumatic brain injury
and normal aging. Brain Cogn 2004;56:43–54.
[54] Mioni G, Stablum F, McClintock SM, Cantagallo A.
Time-based prospective memory in severe traumatic
brain injury patients: the involvement of executive
 revue neurologique 173 (2017) 461–472
functions and time perception. J Int Neuropsychol Soc
2012;18:697–705. http://dx.doi.org/10.1017/
S1355617712000306.
[55] Asloun S, Soury S, Couillet J, Giroire J-M, Joseph P-A,
Mazaux J-M, et al. Interactions between divided attention
and working-memory load in patients with severe
traumatic brain injury. J Clin Exp Neuropsychol
2008;30:481–90. http://dx.doi.org/10.1080/
13803390701550144.
[56] Azouvi P, Jokic C, Van der Linden M, Marlier N, Bussel B.
Working memory and supervisory control after severe
closed-head injury. A study of dual task performance and
random generation. J Clin Exp Neuropsychol 1996;18:317–
37. http://dx.doi.org/10.1080/01688639608408990.
[57] Azouvi P, Couillet J, Leclercq M, Martin Y, Asloun S,
Rousseaux M. Divided attention and mental effort after
severe traumatic brain injury. Neuropsychologia
2004;42:1260–8. http://dx.doi.org/10.1016/
j.neuropsychologia.2004.01.001.
[58] Leclercq M, Couillet J, Azouvi P, Marlier N, Martin Y,
Strypstein E, et al. Dual task performance after severe
diffuse traumatic brain injury or vascular prefrontal
damage. J Clin Exp Neuropsychol 2000;22:339–50. http://
dx.doi.org/10.1076/1380-3395(200006)22 [3;1-V;FT339].
[59] Vallat-Azouvi C, Weber T, Legrand L, Azouvi P. Working
memory after severe traumatic brain injury. J Int
Neuropsychol Soc 2007;13:770–80. http://dx.doi.org/
10.1017/S1355617707070993.
[60] Dobryakova E, Boukrina O, Wylie GR. Investigation of
information flow during a novel working memory task in
individuals with traumatic brain injury. Brain Connect
2015;5:433–41. http://dx.doi.org/10.1089/brain.2014.0283.
[61] Dunning DL, Westgate B, Adlam A-LR. A meta-analysis of
working memory impairments in survivors of moderate-
to-severe traumatic brain injury. Neuropsychology
2016;30:811–9. http://dx.doi.org/10.1037/neu0000285.
[62] Ponsford J, Kinsella G. Attentional deficits following
severe closed head injury. J Clin Exp Neuropsychol
1992;14:822–38.
[63] Van Zomeren AH, Deelman BG. Long term recovery of
visual reaction time after closed head injury. J Neurol
Neurosurg Psychiatry 1978;41:452–7.
[64] Leclercq M, Azouvi P. Attention after traumatic brain
injury. In: Leclercq M, Zimmermann P, editors. Applied
neuropsychology of attention. Hove, UK: Psychology Press;
2002. p. 251–73.
[65] Van Zomeren AH, Brouwer WH. Clinical neuropsychology
of attention. New York: Oxford University Press; 1994.
[66] Whyte J, Grieb-Neff P, Gantz C, Polansky M. Measuring
sustained attention after traumatic brain injury:
differences in key findings from the sustained attention to
response task (SART). Neuropsychologia 2006;44:2007–14.
http://dx.doi.org/10.1016/j.neuropsychologia.2006.02.012.
[67] Spikman J, van Zomeren AH, Deelman BG. Deficits of
attention after closed-head injury: slowness only? J Clin
Exp Neuropsychol 1996;18:755–67.
[68] Whyte J, Polansky M, Fleming M, Coslett HB, Cavallucci C.
Sustained arousal and attention after traumatic brain
injury. Neuropsychologia 1995;33:797–813.
[69] Dockree PM, Bellgrove MA, O’Keeffe FM, Moloney P, Aimola
L, Carton S, et al. Sustained attention in traumatic brain
injury (TBI) and healthy controls: enhanced sensitivity with
dual-task load. Exp Brain Res 2006;168:218–29. http://
dx.doi.org/10.1007/s00221-005-0079-x.
[70] Sinclair KL, Ponsford JL, Rajaratnam SMW, Anderson C.
Sustained attention following traumatic brain injury: use
of the psychomotor vigilance task. J Clin Exp
Neuropsychol 2013;35:210–24. http://dx.doi.org/10.1080/
13803395.2012.762340.
469
[71] Chan RC. Sustained attention in patients with mild
traumatic brain injury. Clin Rehabil 2005;19:188–93.
[72] Veltman JC, Brouwer WH, van Zomeren AH, van
Wolffelaar PC. Central executive aspects of attention in
subacute severe and very severe closed head injury
patients: planning, inhibition, flexibility and divided
attention. Neuropsychology 1996;10:357–67.
[73] Ben-David BM, Nguyen LLT, van Lieshout PHHM. Stroop
effects in persons with traumatic brain injury: selective
attention, speed of processing, or color-naming? A meta-
analysis. J Int Neuropsychol Soc 2011;17:354–63. http://
dx.doi.org/10.1017/S135561771000175X.
[74] Ziino C, Ponsford J. Selective attention deficits and
subjective fatigue following traumatic brain injury.
Neuropsychology 2006;20:383–90. http://dx.doi.org/
10.1037/0894-4105.20.3.383.
[75] Dymowski AR, Owens JA, Ponsford JL, Willmott C. Speed of
processing and strategic control of attention after
traumatic brain injury. J Clin Exp Neuropsychol
2015;37:1024–35. http://dx.doi.org/10.1080/
13803395.2015.1074663.
[76] Willmott C, Ponsford J, Hocking C, Schönberger M. Factors
contributing to attentional impairments after traumatic
brain injury. Neuropsychology 2009;23:424–32. http://
dx.doi.org/10.1037/a0015058.
[77] Ponsford J, Kinsella G. The use of a rating scale of
attentional behaviour. Neuropsychol Rehabil
1991;1:241–57.
[78] Brouwer WH, Ponds RWHM, Van Wolffelaar PC, Van
Zomeren AH. Divided attention 5 to 10 years after severe
closed head injury. Cortex 1989;25:219–30.
[79] Spikman JM, Deelman BG, van Zomeren AH. Executive
functioning, attention and frontal lesions in
patients with chronic CHI. J Clin Exp Neuropsychol
2000;22:325–38.
[80] McDowell S, Whyte J, D’Esposito M. Working memory
impairments in traumatic brain injury: Evidence from a
dual-task paradigm. Neuropsychologia 1997;35:1341–53.
[81] Park NW, Moscovitch M, Robertson IH. Divided attention
impairments after traumatic brain injury.
Neuropsychologia 1999;37:1119–33.
[82] Mathias JL, Wheaton P. Changes in attention and
information-processing speed following severe traumatic
brain injury: a meta-analytic review. Neuropsychology
2007;21:212–23. http://dx.doi.org/10.1037/0894-
4105.21.2.212.
[83] Belmont A, Agar N, Hugeron C, Gallais B, Azouvi P. Fatigue
and traumatic brain injury. Ann Readapt Med Phys
2006;49:283–8. http://dx.doi.org/10.1016/
j.annrmp.2006.04.017 [370–4].
[84] Bushnik T, Englander J, Wright J. Patterns of fatigue and its
correlates over the first 2 years after traumatic brain
injury. J Head Trauma Rehabil 2008;23:25–32. http://
dx.doi.org/10.1097/01.HTR. 0000308718.88214.bb.
[85] Englander J, Bushnik T, Oggins J, Katznelson L. Fatigue
after traumatic brain injury: association with
neuroendocrine, sleep, depression and other factors. Brain
Inj 2010;24:1379–88. http://dx.doi.org/10.3109/
02699052.2010.523041.
[86] Ponsford JL, Ziino C, Parcell DL, Shekleton JA, Roper M,
Redman JR, et al. Fatigue and sleep disturbance following
traumatic brain injury–their nature, causes, and potential
treatments. J Head Trauma Rehabil 2012;27:224–33. http://
dx.doi.org/10.1097/HTR.0b013e31824e1a8.
[87] Van Zomeren A, Brouwer WH, Deelman BG. Attentional
deficits: the riddles of selectivity, speed, and alertness. In:
Brooks D, editor. Closed Head Inj Psychol Soc Fam
Consequences. Oxford: Oxford University Press; 1984. p.
74–107.
470 revue neurologique 173 (2017) 461–472
[88] Ziino C, Ponsford J. Measurement and prediction of
subjective fatigue following traumatic brain injury. J Int
Neuropsychol Soc 2005;11:416–25.
[89] Ziino C, Ponsford J. Vigilance and fatigue following
traumatic brain injury. J Int Neuropsychol Soc
2006;12:100–10. http://dx.doi.org/10.1017/
S1355617706060139.
[90] Belmont A, Agar N, Azouvi P. Subjective fatigue, mental
effort, and attention deficits after severe traumatic brain
injury. Neurorehabil Neural Repair 2009;23:939–44. http://
dx.doi.org/10.1177/1545968309340327.
[91] Stuss DT. Traumatic brain injury: relation to executive
dysfunction and the frontal lobes. Curr Opin Neurol
2011;24:584–9. http://dx.doi.org/10.1097/
WCO.0b013e32834c7eb9.
[92] Milner B. Effects of different brain lesions on card sorting:
the role of the frontal lobes. Arch Neurol 1963;9:90–100.
http://dx.doi.org/10.1001/archneur.1963.00460070100010.
[93] Ferland MB, Ramsay J, Engeland C, O’Hara P. Comparison
of the performance of normal individuals and survivors of
traumatic brain injury on repeat administrations of the
Wisconsin Card Sorting Test. J Clin Exp Neuropsychol
1998;20:473–82.
[94] Nelson HE. A modified card sorting test sensitive to frontal
lobe defects. Cortex 1976;12:313–24.
[95] Rapoport MJ, Herrmann N, Shammi P, Kiss A, Phillips A,
Feinstein A. Outcome after traumatic brain injury
sustained in older adulthood: a one-year longitudinal
study. Am J Geriatr Psychiatry 2006;14:456–65. http://
dx.doi.org/10.1097/01.JGP. 0000199339.79689.8a.
[96] Shallice T. Specific impairments of planning. Philos Trans
R Soc Lond B Biol Sci 1982;298:199–209.
[97] Reitan RM. Validity of the trail making test as an indicator
of organic brain damage. Percept Mot Skills 1958;8:271–6.
[98] Dikmen S, Machamer J, Temkin N, McLean A.
Neuropsychological recovery in patients with moderate to
severe head injury: 2 year follow-up. J Clin Exp
Neuropsychol 1990;12:507–19.
[99] Levin HS, Gary Jr HE, Eisenberg HM, Ruff RM, Barth JT,
Kreutzer J, et al. Neurobehavioral outcome 1 year after
severe head injury: experience of the traumatic coma data
bank. J Neurosurg 1990;73:699–709.
[100] Lange RT, Iverson GL, Zakrzewski MJ, Ethel-King PE,
Franzen MD. Interpreting the trail making test following
traumatic brain injury: comparison of traditional time
scores and derived indices. J Clin Exp Neuropsychol
2005;27. http://dx.doi.org/10.1080/1380339049091290.
[101] Draper K, Ponsford J. Cognitive functioning ten years
following traumatic brain injury and rehabilitation.
Neuropsychology 2008;22:618–25. http://dx.doi.org/
10.1037/0894-4105.22.5.618.
[102] Periáñez J, Rı́os-Lago M, Rodrı́guez-Sánchez J, Adrover-
Roig D, Sánchez-Cubillo I, Crespo-Facorro B, et al. Trail
making test in traumatic brain injury, schizophrenia, and
normal ageing: sample comparisons and normative data.
Arch Clin Neuropsychol 2007;22:433–47.
[103] Levin HS, Goldstein FC, Willliams DH, Eisenberg HM. The
contribution of frontal lobe lesions to the neurobehavioral
outcome of closed head injury. In: Levin HS, Eisenberg HM,
Benton AL, editors. Frontal lobe function and dysfunction.
New York: Oxford University Press; 1991. p. 318–38.
[104] Henry JD, Crawford JR. A meta-analytic review of verbal
fluency performance in patients with traumatic brain
injury. Neuropsychology 2004;18:621–8. http://dx.doi.org/
10.1037/0894-4105.18.4.621.
[105] Stroop JR. Studies of interference in serial verbal reactions.
J Exp Psychol 1935;18:643–62.
[106] Fortin S, Godbout L, Braun CM. Cognitive structure of
executive deficits in frontally lesioned head trauma
patients performing activities of daily living. Cortex
2003;39:273–91.
[107] Cantin JF, McFadyen BJ, Doyon J, Swaine B, Dumas D,
Vallee M. Can measures of cognitive function predict
locomotor behaviour in complex environments following
a traumatic brain injury? Brain Inj 2007;21:327–34. http://
dx.doi.org/10.1080/02699050701209972.
[108] Vakil E, Weisz H, Jedwab L, Groswasser Z, Aberbuch S.
Stroop color-word task as a measure of selective
attention: efficiency in closed-head-injured patients. J Clin
Exp Neuropsychol 1995;17:335–42.
[109] Kennedy MR, Wozniak JR, Muetzel RL, Mueller BA, Chiou
HH, Pantekoek K, et al. White matter and neurocognitive
changes in adults with chronic traumatic brain injury.
J Int Neuropsychol Soc 2009;15:130–6. http://dx.doi.org/
10.1017/S1355617708090024.
[110] Shallice T, Burgess P. Deficits in strategy application
following frontal lobe damage in man. Brain 1991;114:
727–41.
[111] Boyd TM, Sautter SW. Route finding: a measure of
everyday executive functioning in the head-injured adult.
Appl Cogn Psychol 1993;7:171–81.
[112] Cazalis F, Azouvi P, Sirigu A, Agar N, Burnod Y. Script
knowledge after severe traumatic brain injury. J Int
Neuropsychol Soc 2001;7:795–804.
[113] Chevignard MP, Taillefer C, Picq C, Poncet F, Noulhiane M,
Pradat-Diehl P. Ecological assessment of the dysexecutive
syndrome using execution of a cooking task.
Neuropsychol Rehabil 2008;18:461–85.
[114] Chevignard M, Pillon B, Pradat-Diehl P, Taillefer C,
Rousseau S, Le Bras C, et al. An ecological approach to
planning dysfunction: script execution. Cortex
2000;36:649–69.
[115] Spikman JM, Boelen DH, Lamberts KF, Brouwer WH,
Fasotti L. Effects of a multifaceted treatment program for
executive dysfunction after acquired brain injury on
indications of executive functioning in daily life. J Int
Neuropsychol Soc 2010;16:118–29. http://dx.doi.org/
10.1017/S1355617709991020.
[116] Burgess PW, Alderman N, Evans J, Emslie H, Wilson B. The
ecological validity of tests of executive function. J Int
Neuropsychol Soc 1998;4:547–58.
[117] Bennett PC, Ong B, Ponsford J. Measuring executive
dysfunction in an acute rehabilitation setting: using the
dysexecutive questionnaire (DEX). J Int Neuropsychol Soc
2005;11:376–85.
[118] Azouvi P, Vallat-Azouvi C, Joseph P-A, Meulemans T,
Bertola C, Le Gall D, et al. Executive functions deficits after
severe traumatic brain injury: the GREFEX study. J Head
Trauma Rehabil 2015. http://dx.doi.org/10.1097/HTR.
0000000000000169.
[119] McDonald S. Impairments in social cognition following
severe traumatic brain injury. J Int Neuropsychol Soc
2013;19:231–46. http://dx.doi.org/10.1017/
S1355617712001506.
[120] Spikman JM, Timmerman ME, Milders MV, Veenstra WS,
van der Naalt J. Social cognition impairments in relation to
general cognitive deficits, injury severity, and prefrontal
lesions in traumatic brain injury patients. J Neurotrauma
2012;29:101–11. http://dx.doi.org/10.1089/neu.2011.2084.
[121] Spikman JM, Milders MV, Visser-Keizer AC, Westerhof-
Evers HJ, Herben-Dekker M, van der Naalt J. Deficits in
facial emotion recognition indicate behavioral changes
and impaired self-awareness after moderate to severe
traumatic brain injury. PloS One 2013;8:e65581. http://
dx.doi.org/10.1371/journal.pone.0065581.
[122] Milders M, Ietswaart M, Crawford JR, Currie D. Social
behavior following traumatic brain injury and its
association with emotion recognition, understanding of
 revue neurologique 173 (2017) 461–472
intentions, and cognitive flexibility. J Int Neuropsychol Soc
2008;14:318–26. http://dx.doi.org/10.1017/
S1355617708080351.
[123] Prigatano GP, Altman IM. Impaired awareness of
behavioral limitations after traumatic brain injury. Arch
Phys Med Rehabil 1990;71:1058–64.
[124] Sherer M, Hart T, Nick TG, Whyte J, Thompson RN, Yablon
SA. Early impaired self-awareness after traumatic brain
injury. Arch Phys Med Rehabil 2003;84:168–76. http://
dx.doi.org/10.1053/apmr.2003.50045.
[125] Robertson K, Schmitter-Edgecombe M. Self-awareness
and traumatic brain injury outcome. Brain Inj 2015;29:848–
58. http://dx.doi.org/10.3109/02699052.2015.1005135.
[126] Ownsworth TL, McFarland K, Young RM. Self-awareness
and psychosocial functioning following acquired brain
injury: An evaluation of a group support programme.
Neuropsychol Rehabil 2000;10:465–84.
[127] Sherer M, Bergloff P, Levin E, High Jr WM, Oden KO, Nick TG.
Impaired awareness and employment outcome after
traumatic brain injury. J Head Trauma Rehabil 1998;13:52–61.
[128] Ownsworth T, Clare L. The association between
awareness deficits and rehabilitation outcome following
acquired brain injury. Clin Psychol Rev 2006;26:783–95.
http://dx.doi.org/10.1016/j.cpr.2006.05.003.
[129] Sherer M, Hart T, Nick TG. Measurement of impaired self-
awareness after traumatic brain injury: a comparison of
the patient competency rating scale and the awareness
questionnaire. Brain Inj 2003;17:25–37.
[130] Ownsworth T, Fleming J, Strong J, Radel M, Chan W, Clare
L. Awareness typologies, long-term emotional adjustment
and psychosocial outcomes following acquired brain
injury. Neuropsychol Rehabil 2007;17:129–50. http://
dx.doi.org/10.1080/09602010600615506.
[131] Bogod NM, Mateer CA, MacDonald SWS. Self-awareness
after traumatic brain injury: a comparison of measures
and their relationship to executive functions. J Int
Neuropsychol Soc 2003;9:450–8. http://dx.doi.org/10.1017/
S1355617703930104.
[132] Ciurli P, Bivona U, Barba C, Onder G, Silvestro D, Azicnuda
E, et al. Metacognitive unawareness correlates with
executive function impairment after severe traumatic
brain injury. J Int Neuropsychol Soc 2010;16:360–8. http://
dx.doi.org/10.1017/S135561770999141X.
[133] Fleming J, Strong J, Ashton R. Self-awareness of deficits in
adults with traumatic brain injury: How best to measure?
Brain Inj 1996;10:1–15.
[134] Bivona U, Riccio A, Ciurli P, Carlesimo GA, Delle Donne V,
Pizzonia E, et al. Low self-awareness of individuals with
severe traumatic brain injury can lead to reduced ability to
take another person’s perspective. J Head Trauma Rehabil
2014;29:157–71. http://dx.doi.org/10.1097/
HTR.0b013e3182864f0b.
[135] Morton N, Barker L. The contribution of injury severity,
executive and implicit functions to awareness of deficits
after traumatic brain injury (TBI). J Int Neuropsychol Soc
2010;16:1089–98. http://dx.doi.org/10.1017/
S1355617710000925.
[136] Ponsford J, Draper K, Schonberger M. Functional outcome
10 years after traumatic brain injury: its relationship with
demographic, injury severity, and cognitive and
emotional status. J Int Neuropsychol Soc 2008;14:233–42.
http://dx.doi.org/10.1017/S1355617708080272.
[137] Benedictus MR, Spikman JM, van der Naalt J. Cognitive and
behavioral impairment in traumatic brain injury related to
outcome and return to work. Arch Phys Med Rehabil
2010;91:1436–41. http://dx.doi.org/10.1016/
j.apmr.2010.06.019.
[138] Ponsford JL, Olver JH, Curran C. A profile of outcome: 2
years after traumatic brain injury. Brain Inj 1995;9:1–10.
471
[139] Ciurli P, Formisano R, Bivona U, Cantagallo A, Angelelli P.
Neuropsychiatric disorders in persons with severe
traumatic brain injury: prevalence, phenomenology,
and relationship with demographic, clinical, and
functional features. J Head Trauma Rehabil
2011;26:116–26. http://dx.doi.org/10.1097/
HTR.0b013e3181dedd0e.
[140] Bayen E, Jourdan C, Ghout I, Darnoux E, Azerad S, Vallat-
Azouvi C, et al. Objective and subjective burden of
informal caregivers 4 years after a severe traumatic brain
injury: results from the Paris-TBI study. J Head Trauma
Rehabil 2014. http://dx.doi.org/10.1097/
HTR.0000000000000079.
[141] Bayen E, Pradat-Diehl P, Jourdan C, Ghout I, Bosserelle V,
Azerad S, et al. Predictors of informal care burden 1 year
after a severe traumatic brain injury: results from the
Paris-TBI study. J Head Trauma Rehabil 2013;28:408–18.
http://dx.doi.org/10.1097/HTR.0b013e31825413cf.
[142] Brooks N. Personality change after severe head injury.
Acta Neurochir (Wien) 1988;44:59–64.
[143] Arnould A, Dromer E, Rochat L, Van der Linden M, Azouvi
P. Neurobehavioral and self-awareness changes after
traumatic brain injury: towards new multidimensional
approaches. Ann Phys Rehabil Med 2016;59:18–22. http://
dx.doi.org/10.1016/j.rehab.2015.09.002.
[144] Arnould A, Rochat L, Azouvi P, Van der Linden M. A
multidimensional approach to apathy after traumatic
brain injury. Neuropsychol Rev 2013;23:210–33. http://
dx.doi.org/10.1007/s11065-013-9236-3.
[145] Rochat L, Beni C, Annoni J-M, Vuadens P, Van der Linden
M. How inhibition relates to impulsivity after moderate to
severe traumatic brain injury. J Int Neuropsychol Soc
2013;19:890–8. http://dx.doi.org/10.1017/
S1355617713000672.
[146] Arnould A, Rochat L, Azouvi P, Van der Linden M.
Apathetic symptom presentations in patients with severe
traumatic brain injury: assessment, heterogeneity and
relationships with psychosocial functioning and
caregivers’ burden. Brain Inj 2015;29:1597–603. http://
dx.doi.org/10.3109/02699052.2015.1075156.
[147] Rochat L, Beni C, Billieux J, Azouvi P, Annoni J-M, Van der
Linden M. Assessment of impulsivity after moderate to
severe traumatic brain injury. Neuropsychol Rehabil
2010;20:778–97. http://dx.doi.org/10.1080/
09602011.2010.495245.
[148] Whiteside SP, Lynam DR. The five factor model and
impulsivity: using a structural model of personality to
understand impulsivity. Personal Individ Differ
2001;30:669–89. http://dx.doi.org/10.1016/S0191-
8869(00)00064-7.
[149] ACRM. Definition of mild traumatic brain injury. J Head
Trauma Rehabil 1993;8:86–7.
[150] Rohling ML, Larrabee GJ, Millis SR. The ‘‘miserable
minority’’ following mild traumatic brain injury: who are
they and do meta-analyses hide them? Clin Neuropsychol
2012;26:197–213. http://dx.doi.org/10.1080/
13854046.2011.647085.
[151] Wood RL. Understanding the ‘‘miserable minority’’: a
diasthesis-stress paradigm for post-concussional
syndrome. Brain Inj 2004;18:1135–53. http://dx.doi.org/
10.1080/02699050410001675906.
[152] Levin HS, Robertson CS. Mild traumatic brain injury in
translation. J Neurotrauma 2013;30:610–7. http://
dx.doi.org/10.1089/neu.2012.2394.
[153] Meares S, Shores EA, Taylor AJ, Batchelor J, Bryant RA,
Baguley IJ, et al. Mild traumatic brain injury does not
predict acute postconcussion syndrome. J Neurol
Neurosurg Psychiatry 2008;79:300–6. http://dx.doi.org/
10.1136/jnnp.2007.126565.
472 revue neurologique 173 (2017) 461–472
[154] Ponsford J, Cameron P, Fitzgerald M, Grant M, Mikocka-
Walus A, Schonberger M. Predictors of postconcussive
symptoms 3 months after mild traumatic brain injury.
Neuropsychology 2012;26:304–13. http://dx.doi.org/
10.1037/a0027888.
[155] Dikmen S, Machamer J, Temkin N. Mild traumatic brain
injury: longitudinal study of cognition. Functional status,
and post-traumatic symptoms. J Neurotrauma 2016.
http://dx.doi.org/10.1089/neu.2016.4618.
[156] De Koning ME, Gareb B, El Moumni M, Scheenen ME, van
der Horn HJ, Timmerman ME, et al. Subacute
posttraumatic complaints and psychological distress in
trauma patients with or without mild traumatic brain
injury. Injury 2016;47:2041–7. http://dx.doi.org/10.1016/
j.injury.2016.04.036.
[157] Hartvigsen J, Boyle E, Cassidy JD, Carroll LJ. Mild traumatic
brain injury after motor vehicle collisions: what are the
symptoms and who treats them? A population-based 1-
year inception cohort study. Arch Phys Med Rehabil
2014;95:S286–94. http://dx.doi.org/10.1016/
j.apmr.2013.07.029.
[158] McMahon P, Hricik A, Yue JK, Puccio AM, Inoue T, Lingsma
HF, et al. Symptomatology and functional outcome in mild
traumatic brain injury: results from the prospective
TRACK-TBI study. J Neurotrauma 2014;31:26–33. http://
dx.doi.org/10.1089/neu.2013.2984.
[159] Ponsford J, Willmott C, Rothwell A, Cameron P, Kelly AM,
Nelms R, et al. Factors influencing outcome following mild
traumatic brain injury in adults. J Int Neuropsychol Soc
2000;6:568–79.
[160] Whittaker R, Kemp S, House A. Illness perceptions and
outcome in mild head injury: a longitudinal study.
J Neurol Neurosurg Psychiatry 2007;78:644–6. http://
dx.doi.org/10.1136/jnnp.2006.101105.
[161] Gunstad J, Suhr JA. Perception of illness: nonspecificity of
postconcussion syndrome symptom expectation. J Int
Neuropsychol Soc 2002;8:37–47.
[162] Bryant R. Post-traumatic stress disorder vs traumatic
brain injury. Dialogues Clin Neurosci 2011;13:251–62.
[163] Silverberg ND, Gardner AJ, Brubacher JR, Panenka WJ, Li JJ,
Iverson GL. Systematic review of multivariable prognostic
models for mild traumatic brain injury. J Neurotrauma
2015;32:517–26. http://dx.doi.org/10.1089/neu.2014.3600.
[164] Binder LM, Rohling ML, Larrabee J. A review of mild head
trauma. Part I: meta-analytic review of neuropsychological
studies. J Clin Exp Neuropsychol 1997;19:421–31.
[165] Vanderploeg RD, Curtiss G, Belanger HG. Long-term
neuropsychological outcomes following mild traumatic
brain injury. J Int Neuropsychol Soc 2005;11:228–36. http://
dx.doi.org/10.1017/S1355617705050289.
[166] Belanger HG, Curtiss G, Demery JA, Lebowitz BK,
Vanderploeg RD. Factors moderating neuropsychological
outcomes following mild traumatic brain injury: a meta-
analysis. J Int Neuropsychol Soc 2005;11:215–27.
[167] Dean PJA, Sterr A. Long-term effects of mild traumatic
brain injury on cognitive performance. Front Hum
Neurosci 2013;7:30. http://dx.doi.org/10.3389/
fnhum.2013.00030.
[168] Jourdan C, Bayen E, Vallat-Azouvi C, Ghout I, Darnoux E,
Azerad S, et al. Late functional changes post-severe
traumatic brain injury are related to community re-entry
support: results from the Paris-TBI cohort. J Head Trauma
Rehabil 2017. http://dx.doi.org/10.1097/
HTR0000000000000276.