You are on page 1of 17

J Head Trauma Rehabil

Vol. 29, No. 4, pp. 321–337


c 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins
Copyright 

INCOG Recommendations for


Management of Cognition Following
Traumatic Brain Injury, Part II: Attention
and Information Processing Speed
Jennie Ponsford, MA, PhD; Mark Bayley, MD; Catherine Wiseman-Hakes, PhD;
Leanne Togher, BAppSc, PhD; Diana Velikonja, PhD; Amanda McIntyre, MSc;
Shannon Janzen, MSc; Robyn Tate, PhD, On Behalf of the INCOG Expert Panel

Introduction: Traumatic brain injury, due to its diffuse nature and high frequency of injury to frontotemporal and
midbrain reticular activating systems, may cause disruption in many aspects of attention: arousal, selective atten-
tion, speed of information processing, and strategic control of attention, including sustained attention, shifting and
dividing of attention, and working memory. An international team of researchers and clinicians (known as INCOG)
convened to develop recommendations for the management of attentional problems. Methods: The experts se-
lected recommendations from published guidelines and then reviewed literature to ensure that recommendations
were current. Decision algorithms incorporating the recommendations based on inclusion and exclusion criteria of
published trials were developed. The team then prioritized recommendations for implementation and developed
audit criteria to evaluate adherence to these best practices. Results: The recommendations and discussion highlight
that metacognitive strategy training focused on functional everyday activities is appropriate. Appropriate use of dual
task training, environmental modifications, and cognitive behavioral therapy is also discussed. There is insufficient
evidence to support mindfulness meditation and practice on de-contextualized computer-based tasks for attention.
Administration of the medication methylphenidate should be considered to improve information-processing speed.
Conclusion: The INCOG recommendations for rehabilitation of attention provide up-to-date guidance for clini-
cians treating people with traumatic brain injury. Key words: attention, cognitive rehabilitation, information processing,
traumatic brain injury

Author Affiliations: NHMRC Centre of Research Excellence in


Traumatic Brain Injury Psychosocial Rehabilitation, Canberra, Australia
(Drs Ponsford, Togher, and Tate); School of Psychological Sciences,
Monash University and Epworth Hospital, Melbourne, Australia
I N 1890, William James1 defined attention as, “the
taking possession of the mind, in clear and vivid
form, of one out of what may seem several simulta-
(Dr Ponsford); National Trauma Research Institute, Monash University
and the Alfred Hospital, Melbourne, Australia (Dr Ponsford); Neuro neously possible objects or trains of thought . . . . It
Rehabilitation Program, Toronto Rehabilitation Institute, University of implies withdrawal from some things in order to deal
Toronto, Toronto, Canada (Dr Bayley); Bloorview Research Institute, effectively with others.”(pp403–404) Attention is clearly a
Holland Bloorview Kids Rehabilitation Hospital, Toronto, Canada
(Dr Wiseman-Hakes); Speech Pathology, Faculty of Health Sciences, The multifaceted construct.2 Attentional processes are me-
University of Sydney, New South Wales, Australia (Dr Togher); diated by diffuse networks, including the dopaminergic
Neuropsychology, Acquired Brain Injury Program, Hamilton Health and noradrenergic afferent pathways to the dorsolateral
Sciences, Hamilton, Ontario, Canada (Dr Velikonja); Department of
Psychiatry and Behavioural Neurosciences, DeGroote School of Medicine, prefrontal cortex, parietal lobes, and thalamic projec-
McMaster University, Hamilton, Ontario, Canada (Ms Velikonja); tion system.3,4 Theoretical models of attention suggest
Lawson Health Research Institute, London, Canada (Mss McIntyre and that attentional functions are mediated by several
Janzen); Royal Rehabilitation Centre Sydney, New South Wales,
Australia (Dr Tate); and Centre for Rehabilitation Research, Kolling
Institute, Sydney Medical School—Northern, University of Sydney, The authors declare no conflicts of interest.
Australia (Dr Tate).
Corresponding Author: Jennie Ponsford, MA, PhD, School of Psycho-
The authors gratefully acknowledge the support of the Victorian Transport logical Sciences, Monash University, Clayton, 3800, Victoria, Aistralia
Accident Commission (TAC) through its Victorian Neurotrauma Initia- (jennie.ponsford@monash.edu).
tive (VNI), Monash University, and the Ontario Neurotrauma Foundation
(ONF) for their support of this project. DOI: 10.1097/HTR.0000000000000072

321

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
322 JOURNAL OF HEAD TRAUMA REHABILITATION/JULY–AUGUST 2014

interconnected networks, including a sensory selective processing,13–15 working memory difficulties,16 im-
attentional system, mediated by the parieto-temporo- paired levels of vigilance or sustained attention
occipital area, responsible for orienting, engaging, and performance,17,18 difficulty dividing attention under
disengaging attention and object recognition; a system conditions of high working memory load,14,19,20 be-
controlling arousal, sustained attention, and vigilance, also havioral distraction,21 and problems with goal-directed
regulating mood, motivation, the salience of stimuli and allocation of attention on tasks with multiple steps or
readiness to respond, mediated by the midbrain reticular changing demands.22,23
activating system, and limbic structures; and an anterior It is, therefore, not surprising, based on subjective re-
system for selection and control of responses, involving inten- ports, that attentional difficulties are among the most
tional and strategic control, switching and inhibition, common cognitive sequelae of TBI, being reported by
mediated by the frontal lobes, anterior cingulate gyrus, more than 60% of individuals with moderate to severe
and basal ganglia, with the thalamus relaying incoming injuries as long as 10 years postinjury.24–26 They may
information and outgoing responses.5–7 also be associated with mild TBI.27,28 When completing
There is debate as to how to describe the component a Rating Scale of Attentional Behavior, clinicians and
processes of attention; Whyte et al2 suggests that they relatives most commonly endorse problems in the do-
include arousal, selection, strategic control, and processing mains of processing speed, sustaining attention, paying
speed. A number of theoretical models have contributed attention to more than 1 thing at a time, ignoring distrac-
to the characterization of components of attention. Ac- tions, and missing details.29 Attentional impairments
cording to van Zomeren and Brouwer,8 intensity in- contribute to difficulty engaging in important life roles
volves arousal, alertness, attentional capacity, and vigi- such as work or study and also affect social interaction.24
lance, whereas selectivity involves the process of filtering They may also be associated with anxiety after TBI,30 as
relevant sensory information from irrelevant material, well as fatigue31 and sleep-wake disturbances.32 There-
sometimes on spatial grounds. Shiffrin and Schneider9 fore, improving or maximizing attention represents an
proposed that attention was mediated by 2 parallel pro- important goal of the rehabilitation process. However,
cesses: automatic processing, which is parallel in nature, despite a plethora of studies, the evidence supporting
and unaffected by load, and controlled processing, which specific intervention strategies remains limited.
is serial in nature and, therefore, has a limited rate and ca-
pacity. The duration of controlled processing is affected
METHODS
by the cognitive steps required by a task8 and the speed
of information processing. Baddeley’s10 process of working The Guidelines Adaptation and Development
memory allows for temporary storage and manipulation (ADAPTE) process was used to develop the INCOG
during controlled information processing. Allocation of guidelines,33,34 with INCOG being an acronym stand-
attentional resources when performing complex tasks ing for “International Cognitive.” An international ex-
is said to be controlled by a “central executive,” akin pert panel was formed through invitations of authors of
to Shallice’s11 concept of supervisory attentional control. previously published cognitive rehabilitation guidelines
These executive processes exercise what Whyte et al2 and contacts of the team. In preparation, a detailed In-
term strategic control over controlled processing includ- ternet and Medline search was conducted to identify
ing the ability to maintain attention to a task; inhibit published TBI and cognitive rehabilitation evidence-
disruption by distracting influences; shift attention in based guidelines.35 The quality of the development pro-
line with changing goals and priorities; manipulate in- cess for each eligible clinical practice guideline (CPG)
formation currently held in mind (referred to as working was evaluated using the Appraisal of Guidelines for Re-
memory); and divide attention between 2 or more task search and Evaluation (AGREE II) instrument.36,37 The
demands. Thus, the components of attention consid- ADAPTE process involves extracting recommendations
ered “in scope” for this review include arousal, selective from these CPGs to allow easy comparison, for exam-
attention, speed of information processing, and strategic con- ple, all recommendations about executive function were
trol of attention, including sustained attention, shifting and tabulated together. The Evidence-Based Review of Ac-
dividing of attention, and working memory. quired Brain Injury (ERABI: http://www.abiebr.com/)
Arguably, traumatic brain injury (TBI) may disrupt synopses of evidence for each topic area were also dis-
any or all of these processes, given its diffuse nature tributed to the panel.38
and high frequency of injury to frontotemporal and The initial expert panel meeting was scheduled for
midbrain reticular activating systems. Diffuse axonal convenience just prior to the World Congress of Neu-
injury potentially disrupts attentional neural networks, rorehabilitation in Melbourne, Australia, in May of
including ascending noradrenergic, dopaminergic, 2012. Some members attended via Web conferencing
and serotonergic pathways.12 Experimental studies from the United States and Canada. This panel exam-
have confirmed the presence of slowed information ined the recommendations matrix and selected suitable

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
INCOG Recommendations for Management of Cognition Following TBI 323

recommendations from existing guidelines or articu- of the experts was asked in this exercise to vote for his
lated novel recommendations on the basis of the evi- or her top 15 recommendations considering both the
dence available and giving consideration to the clini- importance to practice and feasibility of auditing the
cal applicability of recommendations to achieve mean- recommendations.
ingful outcomes for individuals with TBI. This yielded For each domain of posttraumatic amnesia, attention,
an initial draft set of recommendations; however, to memory, executive function, and cognitive communi-
ensure that the recommendations were updated ac- cation, a clinical algorithm was developed to help clin-
cording to the most current evidence, the research icians decide to whom the recommendations applied.
team prepared synopses of large systematic reviews, the To finalize the algorithm, evidence tables were reviewed
Global Evidence Mapping Initiative,39 based in Aus- to find the inclusion and exclusion criteria for the study
tralia (www.evidencemap.org), the Acquired Brain In- populations that were used. By understanding the sub-
jury Evidence-Based Review38 and PsycBITE (http:// populations of patients with TBI to whom the evidence
www.psycbite.com).40 Furthermore, the reference sec- applies, it is possible to understand what treatments are
tions of all eligible cognitive rehabilitation CPGs were appropriate for each patient. In contrast to other guide-
also extracted. All relevant references were consolidated lines, the INCOG team has identified recommendations
into a reference library that was made available to the au- that could be audited from clinical charts to determine
thor teams as they drafted the manuscripts and finalized adherence to the best practice guidelines in each sec-
the recommendations accordingly. tion. This is known as the INCOG audit tool. A more
By the end, the team completed the evidence review detailed version of the “Methods” section is available in
of more than 600 references found in this search process. the third article of the series.42
Only studies in which more than half of the participants
had TBI were included. This task has resulted in a com- LIMITATIONS OF USE AND DISCLAIMER
prehensive mapping of evidence to all previously and
These recommendations are informed by evidence
newly developed recommendations. The tables will be
for TBI cognitive rehabilitation interventions that was
made available in on online content on the Web site of
current at the time of publication. Relevant evidence
the Journal of Head Trauma Rehabilitation. With the up-
published after the INCOG guideline could influence
dated literature search in mind, the experts graded the
the recommendations contained herein. Clinicians must
evidence. As various systems for determining the level
also consider their own clinical judgment, patient pref-
of evidence were used across the CPGs, the INCOG
erences, and contextual factors such as resource avail-
team standardized this by using the grading system out-
ability in their decision-making processes about imple-
lined later (see Table 1), which was based upon that used
mentation of these recommendations.
in previous guideline development projects.41 These fi-
(Note: The INCOG developers, contributors, and sup-
nal recommendations were then presented to the entire
porting partners shall not be liable for any damages,
team for approval and then the expert panel used Mod-
claims, liabilities, costs, or obligations arising from the
ified Delphi Voting Technique to prioritize the recom-
use or misuse of this material, including loss or damage
mendations from the INCOG guideline for audit. Each
arising from any claims made by a third party.)

RECOMMENDATIONS AND LITERATURE


REVIEW
TABLE 1 INCOG level of evidence-
grading system The reader is referred to the “Methods” article42 of
this series for a complete review of the strategies used
A: Recommendation supported by at least 1 for the literature review and development of the rec-
meta-analysis, systematic review, or randomized ommendations and other tools. The INCOG guidelines
controlled trial of appropriate size with relevant include recommendations relating to best practice in
control group. the remediation of attentional problems following brain
B: Recommendation supported by cohort studies
that at minimum have a comparison group, injury. There have been several previous published re-
well-designed single subject experimental views from which guidelines for the rehabilitation of at-
designs, or small sample size randomized tentional impairments following brain injury have been
controlled trials. recommended. Rees et al43 completed a comprehensive
C: Recommendation supported primarily by expert database search of evidence relating to cognitive reha-
opinion on the basis of their experience through
uncontrolled case series without comparison bilitation for acquired brain injury (ie, cerebrovascular
groups that support the recommendations are accident [CVA], TBI) published 1980–2006, grading ev-
also classified here. idence as Strong if based on 2 or more randomized con-
trolled trials (RCTs), Moderate if based on 1 RCT, Limited
www.headtraumarehab.com

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
324 JOURNAL OF HEAD TRAUMA REHABILITATION/JULY–AUGUST 2014

if based on prospective or retrospective controlled trials Following almost directly from the methods and
or single-group interventions, or Consensus Opinion. In evidence reviewed by Cicerone et al,44 a European Fed-
the domain of attention, they concluded that there was eration of Neurological Societies taskforce47 made the
Strong evidence supporting use of methylphenidate to same practice guideline recommendations for rehabili-
increase speed of information processing, Moderate evi- tation of attention. Another review conducted by the
dence that specific structured training programs had no Academy of Neurologic Communication Disorders by
significant effect on attention in people with moderate Sohlberg et al48 also similarly recommended that re-
to severe brain injury, and that there was Moderate evi- peated stimulation of attention via graded exercises in
dence that dual-task training in speed of processing was conjunction with metacognitive strategy training was
an effective intervention for patients with brain injury. effective for postacute or mildly impaired clients with
A series of reviews led by Cicerone et al44–46 on the intact vigilance.
basis of studies published up to 1997,44 from 1998 to The current guidelines, developed as a basis for an
2002,45 and from 2003 to 2008,46 respectively, graded audit tool to examine clinical practice, differ from the
evidence for rehabilitation following acquired brain in- aforementioned studies in that they are focused on TBI
jury (ie, including both CVA and TBI). Studies rated only, such that studies including only a majority of
as level/class I were based on well-designed prospective participants with TBI were included. Unlike the guide-
RCTs and level/class II were prospective nonrandom- lines by Cicerone et al,44–46 Sohlberg et al,48 and Cappa
ized cohort or retrospective case-control or multiple et al,47 they also included review of pharmacologic inter-
baseline studies. Level/class III included case series with ventions. Moreover, the aforementioned reviews cover
no controls or single subject designs. While the strengths studies published up to 2008 only. The current guide-
and weaknesses of studies are appropriately noted, the lines are based on literature published up to 2012. Four
guidelines in the domain of attention do not separate recommendations are based on level A evidence, 6 rec-
the effects of attention training, in the sense of repeated ommendations are based on level B and/or level C evi-
drill or practice, from studies in which development of dence, and 1 guideline is proposed without supporting
metacognitive strategies are encouraged. Cicerone et al44 evidence. The evidence relating to each guideline is out-
concluded that evidence was insufficient to distinguish lined later.
effects of specific attention training from spontaneous
recovery for people with moderate to severe TBI and NONPHARMACOLOGICAL STRATEGIES TO
stroke during the acute stages of recovery and inpatient ENHANCE ATTENTION
rehabilitation, but that that evidence did support “at-
tention training” during the postacute phase of recov- Attention #1. Metacognitive strategy training using functional
everyday activities should be considered, especially in pa-
ery from TBI or stroke, provided it involved therapist
tients with mild-moderate attention deficits. (Adapted from
monitoring and feedback, teaching of strategies, and was Cicerone et al,
46(p521)
; Sohlberg et al48 ; INCOG Expert Panel42 )
directed at performance on more complex functional
tasks. The manner in which this “Practice Guideline” was There is level A evidence that strategies may be devel-
arrived at was, however, not entirely clear. Following the oped, practised, and applied to compensate for atten-
2005 update, which added 2 class 1 and 1 small class II tional problems, including speed of information pro-
study, Cicerone et al45 recommended as a practice stan- cessing and working memory.
dard, attention training with emphasis on development Fasotti et al49 designed a form of strategy training,
of strategies to compensate for attentional difficulties termed Time Pressure Management (TPM), to enhance
in functional situations in the postacute recovery pe- coping with slowed information processing in individu-
riod. Adding 2 class I and 6 class III studies, Cicerone als with brain injury. This RCT provides level A evidence
et al46 confirmed their practice standard as follows: “Re- in support of the use of strategies to prevent or man-
mediation of attention deficits after TBI should include age time pressure in individuals with TBI and slowed
direct attention training and metacognitive training to processing speed. The 3-step training facilitates aware-
promote development of compensatory strategies and ness of the effects of mental slowness on daily activities,
foster generalization to real world tasks.” A practice op- supports the individual not only in accepting that this
tion stated that: may be a persisting problem but also in realizing that
it is possible to develop and use self-instructional tech-
Computer based interventions may be considered as an ad-
niques, or managing steps prior to or during task per-
junct to clinician-guided treatment for the remediation of formance to reduce time pressure. These might involve,
attention deficits after TBI or stroke. Sole reliance on re- for example, asking for repetition, reducing background
peated exposure and practice on computer-based tasks with- noise, or tape-recording and replaying interactions. The
out some involvement and intervention by a therapist is not implementation of steps is demonstrated, followed by
recommended. overt self-instruction with written prompts that are

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
INCOG Recommendations for Management of Cognition Following TBI 325

gradually withdrawn and then the strategies are applied as compared with a treatment as usual control condi-
in a range of situations and conditions of increasing tion. Outcomes were assessed on a range of dual tasks.
complexity to encourage generalization. In the RCT, Performance in the walking and talking tasks improved
22 individuals with severe to very severe TBI were ran- significantly in the treated group. These most closely re-
domly assigned to receive TPM or concentration train- sembled the training tasks, which also involved listening
ing, in which verbal instruction was the key element. The and generating verbal responses while walking. No sig-
TPM produced greater gains than concentration training nificant gains were evident on the other dual task activ-
for an information intake task and appeared to general- ities, involving 2 motor or 2 cognitive tasks. This study
ize to other measures of speed and memory function.49 was limited by a lack of blinding in outcome measure-
Winkens et al,50,51 who also demonstrated that these ment. A randomized crossover trial by Couillet et al55
strategies can be learned and applied by patients who evaluated the efficacy of training in dividing attention
had a stroke, highlighted a number of factors that in- between 2 cognitive tasks in 12 patients with severe TBI.
creased chances of successful intervention: some degree Training involved learning to perform each task sepa-
of self-awareness, together with an ability to identify sit- rately and then simultaneously with another task, fol-
uations in which time pressure would cause problems lowing a hierarchy of difficulty. Controls received train-
and to set appropriate goals. Other factors included the ing on other cognitive tasks. A significant training effect
potential for the therapist to apply the training directly was evident on several dual-task measures, each of which
to situations of relevance to the injured individual, as bore some resemblance to the trained tasks, as well as
well as monitor the use of the strategies over time. the divided attention item of the Rating Scale of Atten-
There is level C evidence to suggest that training and tional Behavior. Little effect was evidence on executive
guidance in strategy use may be used to compensate for or working memory measures or on nontarget measures.
problems with divided attention and working memory. Unfortunately, the outcome assessors were not blinded
Cicerone52 provided training in metacognitive strategies to training group in this study either and in fact had also
for increasing efficiency of allocation of attentional re- administered the training. Nevertheless, these 2 studies
sources and management of rate of flow of information suggest that it may be possible to increase dual-tasking
on tasks that demanded divided attention to 4 single skills on specific tasks, which may generalize to similar
cases with mild TBI. This therapy was provided once a tasks in the same modalities. A likely mechanism under-
week for 11 to 27 weeks. It also included explicit dis- pinning the improved performance of dual tasks with
cussion of how to apply the strategies to everyday ac- practice over time is that of automatization, whereby
tivities. There was greater improvement in the treated the conscious attentional demands of a task reduce with
participants on the Paced Auditory Serial Addition Task repetition of the task.56 If this is the mechanism un-
(PASAT) and reduction in self-rated everyday attentional derpinning improvement in task performance, then the
difficulties. Vallat-Azouvi et al53 also reported success underlying impairment in dual-tasking capacity is likely
in training working memory in 2 single cases with se- to remain and become evident on novel tasks. There-
vere TBI undertaking 2 hourly sessions per week over fore, to maximize functional impact from such training,
6 to 8 months. They showed high levels of motivation. it would seem most pragmatic to provide such training
Variability in the nature and severity of cognitive im- on tasks that need to be performed in everyday life.
pairments, the level of self-awareness, and capacity to
Attention #3. Cognitive behaviour therapy techniques should
develop and implement compensatory strategies may
be considered to develop strategies to maximise attention in
underpin the success, or otherwise, of any rehabilitative
individuals with mild to moderate TBI in whom anxiety and
intervention for attention. However, the influence of depression are impacting on attentional function.
these factors has not been systematically studied. There
is also a need for studies examining the extent to which Several studies have highlighted the difficulties in dif-
the frequency and duration of therapy may influence ferentiating symptoms directly associated with the brain
outcome. injury from those due to pain, medication effects, post-
traumatic stress, anxiety, depression, or other stressors,
Attention #2. Training in dual-tasking should be used to im-
prove dual task performance on tasks similar to those trained.
particularly in the case of mild TBI.28,57–60 Since all of
these conditions may contribute to attentional difficul-
Two studies have provided level A evidence in sup- ties, it is clearly important to assess the potential con-
port of the potential for training in multitasking, specif- tribution of these factors and intervene accordingly.61
ically, doing 2 things at once. Evans et al54 evaluated, Psychotherapeutic input to manage psychiatric symp-
in a randomized trial involving 19 people with brain toms may also have beneficial effects on attention.62,63
injury, more than half of whom had TBI, the efficacy of In discussing the management of mild TBI, Mateer
twice-daily practice in exercises combining walking with et al58 and Ruff 59 recommended a cognitive behavioral
cognitive activities with gradually increasing demands, therapy (CBT) approach. The CBT aims to show the
www.headtraumarehab.com

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
326 JOURNAL OF HEAD TRAUMA REHABILITATION/JULY–AUGUST 2014

individuals that their symptoms are common following make alterations to the environment or tasks to reduce
such injuries, that their inner dialogue may be increasing the impact of attentional problems. For example, the
stress levels and associated attentional and other symp- work environment might be altered to reduce distrac-
toms, and equips them with strategies to manage these tions (eg, work in a quiet room, reduce interruptions),
symptoms and take control of their lifestyle. Training in tasks may be altered to reduce the speed or amount of
stress management, relaxation, or meditation techniques information to be processed, prompts may be used to
is also commonly used in these conditions. These con- assist the person to refocus or shift attention to another
siderations and strategies may also be appropriate in aspect of a task, or material may be repeated or made
some individuals with moderate and severe TBI, who available in written form to ensure its comprehension.71
also show high rates of emotional distress following However, no studies have evaluated the use of such
TBI.64,65 An RCT by Tiersky et al66 conducted in indi- strategies to alleviate attentional problems.
viduals with mild and moderate TBI demonstrated sig-
nificantly improved emotional functioning, including Attention #6. Reliance on repeated exposure and practice on
de-contextualized computer based attentional tasks is NOT
lessened anxiety and depression, as well as improved per-
recommended due to lack of demonstrated impact on ev-
formance on a measure of divided attention (PASAT), eryday attentional functions. (Adapted from ABIKUS 2007,
following a combined program of individual CBT of- G42
72(22)
; Cicerone et al
46(p521)
)
fered 3 times per week for 11 weeks and designed to
increase coping skills and decrease stress, as well as cog- Much of the early work in the fields of cognitive re-
nitive remediation. It was not possible to differentiate habilitation focused on the use of training exercises to
the effects of the psychological therapy from that of the ameliorate impairments of attention. In a small series of
cognitive remediation exercises, however. There have single case studies, Wood73 reported improvements in
been no other studies evaluating the impact of CBT on attention to task in response to training and token rein-
attentional functions in individuals with brain injury. forcement. Many of these programs involved computer-
mediated exercises purporting to exercise attentional
Attention #4. Screening for and treatment of co-morbid sleep-
functions.62,74–89 A significant number of these predom-
wake disorders may help to optimize attentional processes.
inantly level C studies, involving samples with TBI, re-
Sleep-wake disorders occur in up to 50% of indi- ported gains on the training tasks, and some also showed
viduals with TBI across all levels of severity. Sleep improvements in performance on other cognitive mea-
and adequate day-time alertness are crucial for opti- sures of attentional function that bore some resem-
mal attention, particularly in the areas of vigilance (sus- blance to the trained task, such as the PASAT.62,86,90,91
tained attention) and speed of processing.67 Some stud- The study with strongest methodology, rated class I by
ies have suggested that sleep-wake disorders exacerbate Cicerone et al,44 was that of Gray et al.77 This RCT in-
impairments in attention post-TBI, and those with poor volving 31 participants, 17 of whom had TBI, found sig-
sleep quality (by self-report) demonstrated significantly nificant gains on the PASAT but not on other cognitive
poorer sustained attention than those with TBI who re- measures of attention on completion of training, but it
ported good quality of sleep.32 There is recent level C did find significant relative gains on the PASAT as well
evidence from a preliminary (small sample size) prospec- as a number of other attentional measures at 6-month
tive single-blind cohort study that treatment of sleep- follow-up in the trained versus untrained groups. There
wake disorders in a sample of adults with chronic mod- was no assessment of everyday attentional behavior.77
erate to severe TBI resulted in statistically significant Sturm et al88 argued for the importance of specificity,
and self-reported improvements in speed of processing, demonstrating differential gains from programs focused
divided auditory attention, and selective attention. Par- on alertness and vigilance, versus those training selective
ticipants in the study also reported improvements in so- and divided attention, but this study focused on indi-
cial, vocational, and academic participation.68 Further viduals with unilateral vascular lesions rather than TBI.
well-designed and controlled studies are needed to fully Novack et al80 found no specific effects from focused
determine the impact of treatment of sleep-wake disor- versus general training in individuals with TBI, and Mid-
ders on attention impairments in those with TBI. dleton et al92 found gains in all cognitive domains re-
gardless of the focus of training. However, many of
Attention #5. Alterations to the environment and tasks may
these evaluative studies did not employ a control group
be used to reduce the impact of attentional problems on daily
activities.
to control for the effects of practice on repeated mea-
sures or spontaneous recovery, and the majority did not
A number of authors have noted that some in- evaluate the extent to which the therapy gains general-
dividuals with TBI have difficulty spontaneously us- ized to impact on the everyday attentional functioning
ing compensatory strategies to alleviate attentional of participants. Those studies that employed a control
problems.69–71 An alternative intervention strategy is to group and evaluated gains in terms of their impact on

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
INCOG Recommendations for Management of Cognition Following TBI 327

attentional function in daily activities did not show viding initial guidance was compared with a computer
greater gains relative to controls.75,83,89,93 training–only condition in terms of impact on perfor-
One well-known computer-mediated program that fo- mance on data entry tasks. Both groups showed a simi-
cuses training on various aspects of attention, includ- lar degree of improvement, and degree of improvement
ing focused, sustained, selective, alternating, and di- was related to use of compensatory strategies. The lack
vided attention, employing auditory and visual exer- of differences between groups suggested that controls
cises, is Attention Process Training (APT), developed had spontaneously adopted many of the same strategies
by Sohlberg and Mateer.86 This has been evaluated in as the strategy training group.
studies with variable methodological rigor, often involv- In summary, there is mixed evidence of efficacy of
ing small numbers of cases.82,86,90,93,94 The largest of repeated practice on de-contextualized tasks, and most
these, a crossover trial involving 14 participants, 12 of positive findings are on neuropsychological measures,
whom had TBI, found increased gains on the PASAT fol- with limited evidence of impact on everyday attentional
lowing treatment with APT compared with brain injury activities. This recommendation is consistent with the
education.90 This study was rated as class I by Cicerone practice option suggested by Cicerone et al.46 There is
et al45 but would rate as level B evidence according to some evidence to suggest that repeated practice on tasks
our classification system because of the small sample size may facilitate the development of strategies that improve
and unblended outcome assessments. Another study by task performance. As recommended in the Attention 1
Park et al82 involving 46 participants found that both guideline, training in compensatory strategies applied
the treated group (using APT) and the nontreated con- to everyday activities should be considered, especially
trol group showed similar gains in performance on the in cases with mild to moderate TBI.
PASAT. Following a meta-analysis of attention training
studies, Park and Ingles81 found that gains were more Attention #7. Training with periodic random auditory alert-
evident in uncontrolled pre-post studies but less so in ing tones for patients with attentional deficits should not be
studies including control groups. They concluded that conducted in therapy outside of a research protocol, as cur-
rent evidence is conflicting. (Adapted from ABIKUS 2007,
training in specific skills might result in improvements 72(p22)
G36)
in that skill, which may also be evident on tasks similar
to those trained but that it could not be assumed that There has been mixed evidence regarding whether
underlying attentional mechanisms were being restored.
self-alerting or external alerting tones can be used to fa-
Findings from another recent series of single case studies
cilitate arousal and self-monitoring in patients with ex-
by Zickefoose et al95 were consistent with this conclu- ecutive dysfunction, who have difficulty planning and
sion. In a meta-analysis, Rohling et al96 corrected for
following through with a course of action. Manly et al98
gains due to practice effects or spontaneous recovery demonstrated that provision of a brief auditory alert-
and found a small though significant effect of atten- ing stimulus, acting as a cue to consider the overall
tion training, but studies included in the review had
goal of the activity, assisted 10 brain injured individ-
predominantly employed neuropsychological outcome uals to monitor their performance and make fewer er-
measures. rors on the multistep “Hotel task,” bringing their perfor-
A factor that may underpin some of the gains ob-
mance to a level that did not differ from that of healthy
served following repeated performance of these exercises controls. On the contrary, in a larger study, Sweeney
is the development of compensatory strategies, such as et al99 found no significant improvement in patients’
chunking, which may enhance the performance on tasks
performance of a virtual reality prospective memory task
used to assess outcome, especially those involving work- that simulated working in a furniture storage unit in re-
ing memory, such as those used by Serino et al.91 They
sponse to periodic auditory alerts, in comparison with
reported success in training of working memory in 9
healthy controls. Thus, there is yet insufficient evidence
people with severe TBI by providing repeated practice to suggest that the use of periodic alerting enhances the
in tasks such as the PASAT and a series of word games
allocation of or switching of attention across different as-
(level B study). Indeed, the most recent version of APT
pects of complex tasks. Other metacognitive approaches
(APT-III) includes increased emphasis on the develop- to support planning, self-monitoring, and execution of
ment of compensatory strategies as part of the training.
complex tasks, such as goal management training, are
It is arguable that gains are made as a result of use of
discussed in the article on rehabilitation of executive
these compensatory strategies, rather than as a result of functioning by Tate et al100 in this series.
restoration of attentional functions. In support of this
contention are the results of a controlled trial by Dirette Attention #8. Training in Mindfulness-based meditation tech-
and Hinojosa,98 using an intervention delivered weekly niques is not recommended for remediation of attention
for 6 weeks. Computerized instruction in verbalization, deficits outside of a research protocol due to lack of demon-
chunking, and pacing with a speech pathologist pro- strated efficacy.
www.headtraumarehab.com

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
328 JOURNAL OF HEAD TRAUMA REHABILITATION/JULY–AUGUST 2014

Some research has also focused on rehabilitation vidual’s self-awareness, motivation, and ability to carry
of sustained attention. This has generally used self- out instructions in a goal-directed manner, which may
instructional techniques. In a level A RCT, McMillan in turn depend on severity of executive impairment.
et al101 evaluated the impact of a brief mindfulness med- These interventions involved individuals with only mild
itation technique, which involved training TBI partic- to moderate executive difficulties. The extent to which
ipants, using an audiotape, to control their attention these factors influence response to these interventions
by concentrating on breathing over extended periods. requires systematic investigation.
After 4 weeks of training, there was no significant reduc-
tion in cognitive failures or improvement on measures PHARMACOLOGICAL STRATEGIES FOR
of attention, memory, or psychological adjustment in IMPROVING ATTENTION
comparison with 2 control groups, which received ei-
ther physical fitness training or no treatment. While the Attention #9. Methylphenidate is recommended to enhance
speed of information processing. (adapted from Warden
authors acknowledged that more intensive training by 106(p1482)
et al).
skilled therapists may have been more effective, this was
not considered feasible within the existing healthcare Given the impact of TBI on neurotransmitter systems
system. underpinning attention, numerous studies have evalu-
There has been some evidence of treatment effects in ated pharmacological interventions. Methylphenidate,
less rigorous studies. Two single case studies have pro- a central nervous system stimulant, increases re-
vided level C evidence that training in self-monitoring of lease and blocks reuptake of dopamine and nora-
slips of attention and identifying their causes, together drenaline, resulting in increased synaptic and extracellu-
with relaxation and use of self-talk strategies for dealing lar concentrations.107 Actions at D1 and α-2-adrenergic
with internal and external distraction, resulted in re- receptors have been linked to the facilitative effects of
duced attentional slips when reading or listening.102,103 methylphenidate on prefrontal cortical modulation of
In a more recent group-based intervention, evaluated in attention and working memory.108 Seven RCTs109–115
a crossover trial, Novakovic-Agopian et al104 trained 16 and 2 case series116,117 have evaluated the effective-
individuals with brain injury of multiple etiologies to ness of methylphenidate in improving attention after
use a range of attentional self-regulation strategies, in- TBI. Four of the RCTs, which are also the 4 largest
cluding mindfulness, to overcome everyday attentional studies, namely, those by Whyte et al,110,112 Willmott
and problem-solving challenges, while receiving brain and Ponsford,109 and Plenger et al113 all showed in-
injury education during a control condition. They found creased cognitive processing speed and attention on
improvements in performance on a range of cognitive neuropsychological tests, when methylphenidate was
measures and reported subjective improvements in per- administered at a dose of 0.3 mg/kg twice daily, al-
sonal functioning, which were not evident following though no significant improvements were noted in di-
an education control condition. However, the method- vided attention, sustained attention, or susceptibility
ology of this level B study was not as strong as that to distraction. Whyte et al110 showed an impact on
in the study by McMillan et al,101 and, in particular, caregiver ratings of everyday attention and Willmott
the impact on everyday functioning over time was not and Ponsford109 showed a positive but nonsignificant
evaluated objectively. Using the same sample as that trend in such ratings. Thus, there is level A evidence
of Novakovic-Agopian and colleagues,104 Chen et al105 supporting use of methylphenidate to increase infor-
used pattern classification to decode individual func- mation processing speed as measured neuropsycholog-
tional magnetic resonance imaging data acquired during ically, with 1 study showing an impact on everyday at-
a visual selective attention task and found significantly tention. However, there has been no investigation of the
enhanced modulation of neural processing in extras- impact of long-term use of methylphenidate by individ-
triate cortex following attention regulation training as uals with TBI. Thus, its impact on activity and partici-
compared with the control condition of education pro- pation is yet to be demonstrated. Dextroamphetamine
vision. Neural changes in prefrontal cortex, which they has been studied in a single case series with reported
suggest is a likely mediator for attention regulation, ap- benefit.118
peared to depend on individual baseline state. How-
ever, given their relatively weaker methodology, these Attention #10. Whilst Amantadine may enhance arousal in
patients in a minimally conscious state, there is little evidence
studies are subject to risk of bias and would need confir-
that it enhances more complex attentional functions following
mation with well-designed controlled studies evaluating emergence from coma.
everyday outcomes. As with the application of any com-
pensatory strategy, the extent to which self-instructional Amantadine is a dopaminergic agent that acts presy-
techniques can be used to enhance arousal and improve naptically to enhance dopamine release and decrease
sustained attention may depend on the injured indi- dopamine reuptake. Although there is level A evidence

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
INCOG Recommendations for Management of Cognition Following TBI 329

that amantadine may enhance arousal in people in a Methylphenidate, administered at 0.3 mg/kg in di-
vegetative or minimally conscious state,119 there is lim- vided doses, has been shown to increase speed of infor-
ited evidence that amantadine enhances more complex mation processing both in inpatients in postacute reha-
attentional functions. Uncontrolled case studies have bilitation and when delivered for up to 6 weeks at longer
suggested that amantadine may improve attention but periods after injury and to enhance everyday attentional
more commonly executive functions.120–122 However, behavior. Although the long-term effects on outcome
these level C studies have been marred by small sam- are not yet known, methylphenidate is indicated for
ples, lack of blinding, and failure to control for practice short-term use to maximize attention in individuals aged
effects. A small placebo controlled study did not find 16 to 60 years who have no history of attention deficit
that amantadine increased the rate of improvement in at- hyperactivity disorder previous stimulant use, drug or
tention and other cognitive functions in the acute stages alcohol dependence, or other psychiatric disorder.
of recovery from TBI123 (level B). More well-controlled Despite their apparent applicability, especially for
studies are required to examine the impact of amanta- individuals without the capacity to implement self-
dine on attention. regulatory strategies, there has been no formal evalua-
Table 2 sets out the guidelines and supporting evi- tion of efficacy of the use of adaptive changes to the envi-
dence. Figure 1 presents the algorithm illustrating rec- ronment or tasks to minimize the impact of attentional
ommended decision-making pathways for managing problems, such as removing noise or other sources of
attentional problems, based on the guidelines. distraction from the home or work environment, or al-
tering tasks to reduce their demands in terms of speed or
multitasking, providing prompting to reorient to tasks,
RECOMMENDED PRACTICE
or using checklists. Addressing other contributing fac-
On the basis of the guidelines, the following practices tors to attentional problems, such as fatigue, sleep-wake
are recommended. Given the high frequency of atten- disturbances, pain, medication effects, and/or anxiety
tional problems in individuals with TBI, it is recom- and depression, also represents important aspects of the
mended that all individuals with moderate to severe TBI intervention process. The outcome of all interventions
have a neuropsychological assessment to determine the should be assessed not only in terms of their impact of
specific nature and extent of their attentional difficul- measures of attentional impairment but also on the indi-
ties. It is also important to investigate the ways in which viduals’ ability to participate in daily activities to which
these attentional problems are manifested and impact- they wish to return.
ing on performance of daily activities. It is acknowledged Table 3 sets out the audit tool items recommended
that this recommendation is based on clinical consen- by the INCOG panel for examining management of
sus. As it is typical of rehabilitation teams to assess a attentional problems in clinical settings.
condition prior to implementing an intervention, the
panel opted to similarly recommend this process for the
DISCUSSION
assessment of attention. The use of everyday measures
such as the Rating Scale of Attentional Behavior29 or Given the high frequency of attentional impairments
the Moss Attention Rating Scale,124 which may be com- following TBI, the identification and treatment of these
pleted by a clinician or a relative, may assist with this. problems is of paramount importance. Despite the de-
It is also important to identify the attentional demands bilitating nature of attentional difficulties in individuals
of the injured individual’s lifestyle and the availability with TBI, there is a lack of established rehabilitation
of environmental supports, as well as factors that may practices to address attention. The evidence in support
be exacerbating attentional problems, including fatigue, of most interventions is not strong. It is recommended
sleep-wake disturbances, pain, medication, anxiety, and that both assessment and intervention not only be fo-
depression. cused on attentional impairments but also be conducted
In implementing therapy to alleviate attentional prob- in the context of the individual’s daily life. Evidence
lems, there is evidence in support of training in metacog- supports training in metacognitive strategies applied to
nitive strategies applied directly to everyday attentional everyday attentional difficulties. Making adjustments to
difficulties. Such strategies might include TPM strate- the environment and tasks undertaken by the injured in-
gies, chunking, or pacing. dividual may also be important, as is addressing fatigue,
There is also support for provision of training in dual sleep-wake disturbances, pain, medication effects, and
tasking, whereby each task is trained separately and then anxiety and depression. Of the pharmacological inter-
together. This may facilitate automatization of task per- ventions available, the strongest evidence is for the use
formance, reducing the burden on a limited conscious of methylphenidate to enhance speed of information
processing capacity of the injured individual. Thus, gains processing in individuals without any history of atten-
may be expected only on trained tasks or similar. tion deficit hyperactivity disorder, stimulant use, drug
www.headtraumarehab.com

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
330

TABLE 2 Recommendation table, attention


Guideline recommendation Grade Reviews RCTs Other
Nonpharmacological interventions for attention/information processing speed
Attention #1
Metacognitive strategy training using functional everyday A Fasotti et al49 Cicerone52
activities should be considered, especially in patients with Vallat-Azouvi et al53
mild-moderate attention deficits.
INCOG (2014)42 /Sohlberg et al48(p37) /Cicerone et al46(p521) (Level
Propose B)
Attention #2
Training in dual tasking should be used to improve dual-task A Couillet et al55
performance on tasks similar to those trained. Evans et al54

Attention #3
Cognitive behavior therapy techniques should be considered to B Tiersky et al66 Mateer et al58
develop strategies to maximize attention in individuals with Ruff59
mild to moderate traumatic brain injury in whom anxiety
depression is impacting on attentional function.
Attention #4
Screening for and treatment of comorbid sleep-wake disorders C Wiseman-Hakes et al68
may help optimize attentional processes.
Attention #5
Alterations to the environment and tasks may be used to C Sloan and Ponsford71
reduce the impact of attentional problems on daily activities
Attention #6
Reliance on repeated exposure and practice on B Park and Ingles81 Dirette and Hinojosa97 Gansler and McCaffrey75
de-contextualized computer-based attentional tasks are NOT Rohling et al96 Gray et al77 Gray and Robertson76
recommended because of lack of demonstrated impact on Malec et al78 Middleton et al92
JOURNAL OF HEAD TRAUMA REHABILITATION/JULY–AUGUST 2014

everyday attentional functions. Niemann et al79 Palmese and Raskin62


ABIKUS G42 p. 22 (2007)78 /Cicerone (2011)51(p521) Novack et al80 Park et al82
Sohlberg et al90 Ponsford and Kinsella83
Robertson et al84
Serino et al91
Sohlberg and Mateer86
Wood73
Zickefoose et al95
(continues)

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
TABLE 2 Recommendation table, attention (Continued)
Guideline recommendation Grade Reviews RCTs Other
Attention #7
Training with periodic random auditory alerting tones for B Manly et al98
patients with attentional deficits should not be conducted in Sweeney et al99
therapy outside of a research protocol, as current evidence is
conflicting.
ABIKUS G36 p. 22 (2007)72
Attention #8
Training in mindfulness-based meditation techniques is not A McMillan et al101 Chen et al105
recommended for remediation of attention deficits outside of Novakovic-Agopian et al104
a research protocol because of lack of demonstrated. Wilson and Robertson102
Webster and Scott103
Pharmacological management for attention/information processing speed
Attention #9
Methylphenidate is recommended to enhance speed of A Gualtieri and Evans114 Bleiberg et al118
information processing. Kim et al111 Kaelin et al116
Warden et al106(p1482) Plenger et al112 Pavlovskaya et al117
Speech et al115
Whyte et al110
Whyte et al112
Willmott and Ponsford109
Attention #10
While amantadine may enhance arousal in patients in a C Kraus and Maki120
minimally conscious state, there is little evidence that it
enhances more complex attentional functions following
emergence from coma.
Kraus et al121
Nickels et al122
Schneider et al123
INCOG Recommendations for Management of Cognition Following TBI

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
www.headtraumarehab.com
331
332

TABLE 3 Audit guidelines for priority recommendations: attentiona


Intervention Assessment of
(guideline Specific activities, need and Patient
recommendation) devices, or tools effectiveness characteristics Discipline
Attention Training
“Metacognitive strategy  Combined with  Assessment for  Mild to moderate  OT
training using functional metacognitive executive need conducted attention deficit  PT
everyday activities should strategy training  Training provided  SLP
be considered, especially in  Functional everyday  MD
patients with activities  Neuro
mild-moderate attention  Environmental  Other
deficits.” (Attention #1) manipulation
 Use of checklists
 Other
Pharmaceutical interventions: Attention
Patient
Drug Used Indication characteristics Found in
Methylphenidate
“Methylphenidate is Yes No  Attentional  Drug charts
recommended to enhance function
speed of information  Speed of cognitive  MD notes
processing.” (Attention #9) processing  Other
 Sustained
JOURNAL OF HEAD TRAUMA REHABILITATION/JULY–AUGUST 2014

attention/vigilance
 Other (please
specify):

a Theaudit tool items that the panel voted as the most important for implementation are listed. It is important to note that many different strategies may be applicable and that the language
used to describe these interventions is likely to vary across settings and cultures.

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
INCOG Recommendations for Management of Cognition Following TBI 333

Impaired attention?
Mild-moderate Training with
impairment metacognitive
strategies applied to
Consider potential medication side-effects (+self-aware) real-world activities
and modify as appropriate.

Dual-task training
Screen for sleep-wake
disturbance Avoid sole use of
computer-mediated
drills

Environmental
Address sleep-wake disturbance Severe
modification
impairment

Time Pressure
Screen for
Management
anxiety and/or
Consider cognitive depression
behavioral therapy for
anxiety and mood Consider
Slow methylphenidate
information
0.3 mg/kg in divided
processing
Assess/consider motivation, doses for up to 6
close other support, (No substance wk
substance use history, and abuse, high
cognitive functions, i.e., self- blood pressure)
awareness, executive and
memory function

Mindfulness techniques and training with periodic random


tones not recommended

Figure 1. Algorithm: Attention. Participant characteristics, measures, and treatments. Studies demonstrating efficacy of interventions
for attentional difficulties in a controlled fashion have been sparse. Those that have demonstrated success in remediating
attentional difficulties by integrating training in performance of attentional tasks with metacognitive or compensatory skills
training have included people with mild to severe injuries, generally aged between 16 and 60 years, and having adequate visual
acuity, hand function, and cognitive function to perform the assessment and training tasks. Participants were generally excluded if
they had other neurological or developmental issues or preexisting psychiatric or substance use problems. They received training
between 3 months and many years after injury. Therefore, it cannot be assumed that other individuals would benefit from these
interventions. Screening measures included a broad range of neuropsychological tests of attention, including the PASAT, Trail
Making Test, cancellation, Digit Span and Digit Symbol substitution tasks, and many others. These tasks have also been used
to evaluate the outcome of interventions. Outcomes have also been measured in terms of subjectively reported changes and
performance on real-world data entry tasks and activity and participation scales. The published studies evaluating the efficacy of
methylphenidate have included individuals with moderate to severe brain injury usually aged 16 to 60 years and having adequate
physical and cognitive abilities to undertake the tasks. While Willmott and Ponsford109 and Kaelin et al116 included patients
in inpatient rehabilitation, others have included individuals more than 6 months postinjury. There was no common attention
measure used to screen for inclusion. Most investigators excluded those with preexisting treatment with methylphenidate, or
substance dependence, concurrent treatment with psychoactive medications, or current drug or alcohol dependence. The most
common outcome was improvement in impairments in processing speed assessed on measures of reaction time and the Symbol
Digit Modalities Tests, but 2 randomized controlled trials included a Rating Scale of Attentional Behavior and 2 case series
reported improvements in function on the Disability Rating Scale.

dependence, or other psychiatric problems. There is both large RCTs, but also well-designed single case stud-
clearly a need for not only much larger studies eval- ies, which allow for a focus on the individuals in the
uating interventions focusing on attentional problems, context of their daily life.

www.headtraumarehab.com

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
334 JOURNAL OF HEAD TRAUMA REHABILITATION/JULY–AUGUST 2014

REFERENCES

1. James W. The Principles of Psychology. Dover Publications Inc; 1890. of executive function: the Virtual Library Task. J Int Neuropsychol
2. Whyte J, Ponsford J, Watanabe T, Hart T. Traumatic brain injury. Soc. 2012;18(3):440–450.
In: Frontera WR, Delisa JD, Gans BM, Walsh NA, Robinson 24. Ponsford JL, Downing M, Olver J, et al. Longitudinal follow-up
L, eds. Delisa’s Physical Medicine and Rehabilitation: Principles and of patients with traumatic brain injury: outcome at 2, 5, and
Practice. 5th ed. Philadelphia, PA: Wolters Kluwer, Lippincott 10-years postinjury. J Neurotrauma. 2014;31(1):64–77.
Williams & Wilkins; 2010:575–623. 25. Himanen L, Portin R, Isoniemi H, Helenius H, Kurkj T, Tenovuo
3. Amsten AF, Robbings TW. Neurochemical modulation of pre- O. Longitudinal cognitive changes in traumatic brain injury: a
frontal cortical function in humans and animals. In: Stuss DT, 30-year follow-up study. Neurology. 2006;66:187–192.
Knight RT, eds. Principles of Frontal Lobe Function. New York, NY: 26. Hoofien D, Gilboa A, Vakil E, Donovick PJ. Traumatic brain
Oxford University Press; 2002:51–84. injury 10–20 years later: a comprehensive outcome study of psy-
4. McAllister TW, Flashman LA, Sparling MB, Saykin AJ. Work- chiatric symptomatology, cognitive abilities, and psychosocial
ing memory deficits after traumatic brain injury: catecholaminer- functioning. Brain Inj. 2001;15:189–209.
gic mechanisms and prospects for treatment—a review. Brain Inj. 27. Ponsford J, Willmott C, Rothwell A, et al. Factors influencing
2004;18(4):331–350. outcome following mild traumatic brain injury in adults. J Int
5. Posner MI, Rothbart MK. Attentional mechanisms and conscious Neuropsychol Soc. 2000;6(5):568–579.
experience. In: Milner AD, Rugg MD, eds. The Neuropsychology of 28. Carroll LJ, Cassidy JD, Peloso PM, et al. Prognosis for mild
Consciousness. London: Academic Press; 1992:91–112. traumatic brain injury: results of the WHO Collaborating Cen-
6. Stuss DT, Benson DF. The Frontal Lobes. New York, NY: Raven tre Task Force on Mild Traumatic Brain Injury. J Rehabil Med.
Press; 1986. 2004(43 suppl):84–105.
7. Cohen RA. The Neuropsychology of Attention. New York, NY: 29. Ponsford JL, Kinsella G. The use of a Rating Scale of Attentional
Plenum Press; 1993. Behaviour. Neuropsychol Rehabil. 1991;1:241–257.
8. Van Zomeren AH, Brouwer WH. Clinical Neuropsychology of At- 30. Gould KR, Ponsford JL, Spitz G. Contributions of cognitive
tention. New York, NY: Oxford University Press; 1994. impairments to anxiety disorder following traumatic brain injury.
9. Shiffrin RM, Schneider WM. Controlled and automatic human J Clin Exp Neuropsychol. In press.
information processing: II. Perceptual learning, automatic attend- 31. Ziino C, Ponsford J. Selective attention deficits and subjec-
ing, and a general theory. Psychol Rev. 1977;84(2):127–190. tive fatigue following traumatic brain injury. Neuropsychology.
10. Baddeley AD. Working Memory. Oxford: Claredon Press; 2006;20(3):383–390.
1986. 32. Bloomfield ILM, Espie CA, Evans JJ. Do sleep difficulties exac-
11. Shallice T. Specific impairments in planning. In: Broadbent erbate deficits in sustained attention following traumatic brain
DE, Weiskrantz L, eds. The Neuropsychology of Cognitive Function. injury? J Int Neuropsychol Soc. 2010;16:17–25.
London: The Royal Society; 1982:199–209. 33. ADAPTE Collaboration. The ADAPTE Process: Resource Toolkit for
12. Povlishock J, Katz D. Update of neuropathology and neurologi- Guideline Adaptation. Version 2.0 ed. 2009. http://www.g-i-n.net.
cal recovery after traumatic brain injury. J Head Trauma Rehabil. Accessed January 29, 2014.
2005;20(1):76–94. 34. Graham ID, Harrison MB. Evaluation and adaptation of clinical
13. Spikman JM, van Zomeren AH, Deelman BG. Deficits of at- practice guidelines. Evidence Based Nurs. 2005;8(3):68–72.
tention after closed-head injury: slowness only? J Clin Exp 35. Bragge P PL, Marshall S, et al. Quality of guidelines for cognitive
Neuropsychol. 1996;18(5):755–767. rehabilitation following traumatic brain injury. J Head Trauma
14. Willmott C, Ponsford J, Hocking C, Schönberger M. Factors con- Rehabil. 2014;29(4):277–289.
tributing to attentional impairments following traumatic brain 36. Appraisal of Guidelines Research & Evaluation. AGREE: advanc-
injury. Neuropsychology. 2009;23(4):424–432. ing the science of practice guidelines. http://www.agreetrust.org/.
15. Ponsford JL, Kinsella G. Attentional deficits following closed- Published 2014. Accessed January 2012.
head injury. J Clin Exp Neuropsychol. 1992;14(5):822–838. 37. Brouwers MC, Kho ME, Browman GP, et al. AGREE II: advanc-
16. Vallat-Azouvi C, Weber T, Legrand L, Azouvi P. Working mem- ing guideline development, reporting and evaluation in health
ory after severe traumatic brain injury. J Int Neuropsychol Soc. care. CMAJ. 2010;182(18):E839–E842.
2007;13(5):770–780. 38. Teasell R, Bayona N, Marshall S, et al. A systematic review of
17. Ziino C, Ponsford J. Vigilance and fatigue following traumatic the rehabilitation of moderate to severe acquired brain injuries.
brain injury. J Int Neuropsychol Soc. 2006;12:100–110. Brain Inj. 2007;21(2):107–112.
18. Robertson IH, Manly T, Andrade H, Baddeley BI, Yiend J. 39. Bragge P, Clavisi O, Turner T, Tavender E, Collie A, Gruen
‘Oops!’ Performance correlates of everyday attentional failures RL. The Global Evidence Mapping Initiative: scoping research
in traumatic brain injured and normal subjects. Neuropsychology. in broad topic areas. BMC Med Res Methodol. 2011;11:92.
1997;35:747–758. 40. Tate R, Perdices M, McDonald S, et al. Development of a
19. Asloun S, Soury S, Couillet J, et al. Interactions between divided database of rehabilitation therapies for the psychological con-
attention and working-memory load in patients with severe trau- sequences of acquired brain impairment. Neuropsychol Rehabil.
matic brain injury. J Clin Exp Neuropsychol. 2008;30(4):481–490. 2004;14(5):517–534.
20. Azouvi P, Vallat-Azouvi C, Belmont A. Cognitive deficits after 41. Lindsay P, Bayley M, Hellings C, Hill M, Woodbury E, Phillips S.
traumatic coma. Prog Brain Res. 2009;177:89–110. Canadian best practice recommendations for stroke care (updated
21. Whyte J, Fleming M, Polansky M, Cavallucci C, Coslett HB. The 2008). CMAJ. 2008;179(12):S1–25.
effects of visual distraction following traumatic brain injury. J Int 42. Bayley M, Tate R, Douglas J, et al. INCOG guidelines for cogni-
Neuropsychol Soc. 1998;4:127–136. tive rehabilitation following traumatic brain injury: methods and
22. Shallice T, Burgess PW. Deficits in strategy application following overview. J Head Trauma Rehabil. 2014;29(4):290–306.
frontal lobe damage in man. Brain. 1991;114(2):727–741. 43. Rees L, Marshall S, Hartridge C, Mackie D, Weiser M.
23. Renison B, Ponsford J, Testa R, Richardson B, Brownfield K. The Cognitive interventions post acquired brain injury. Brain Inj.
ecological and construct validity of a newly developed measure 2007;21(2):161–200.

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
INCOG Recommendations for Management of Cognition Following TBI 335

44. Cicerone KD, Dahlberg C, Kalmar K, et al. Evidence-based cog- comes following traumatic brain injury. JAMA. 2010;303:1938–
nitive rehabilitation: recommendations for clinical practice. Arch 1945.
Phys Med Rehabil. 2000;81(12):1596–1615. 66. Tiersky LA, Anselmi V, Johnston MV, et al. A trial of neuropsy-
45. Cicerone KD, Dahlberg C, Malec JF, et al. Evidence-based cog- chologic rehabilitation in mild-spectrum traumatic brain injury.
nitive rehabilitation: updated review of the literature from 1998 Arch Phys Med Rehabil. 2005;86:1565–1574.
through 2002. Arch Phys Med Rehabil. 2005;86(8):1681–1692. 67. Banks S, Dinges DF. Behavioral and physiological consequences
46. Cicerone KD, Langenbahn DM, Braden C, et al. Evidence- of sleep restriction. J Clin Sleep Med. 2007;3:519–528.
based cognitive rehabilitation: updated review of the literature 68. Wiseman-Hakes C, Murray BJ, Moineddin R, et al. Evaluating the
from 2003 through 2008. Archf Phys Med Rehabil. 2011;92(4): impact of treatment for trauma related sleep/wake disorders on
519–530. recovery of cognition and communication in adults with chronic
47. Cappa SF, Benke T, Clarke S, Rossi B, Stemmer B, van Heugten TBI. Brain Inj. 2013;27(12):1364–1376.
CM. EFNS guidelines on cognitive rehabilitation: report of an 69. Neistadt ME. The neurobiology of learning: implications for
EFNS task force. Eur J Neurol. 2003;10(1):11–23. treatment of adults with brain injury. Am J Occup Ther.
48. Sohlberg MM, Avery J, Kennedy MRT, et al. Practice guide- 1994;48:421–430.
lines for direct attention training. J Med Speech-Lang Pathol. 70. Sohlberg MM, Raskin SA. Principles of generalization applied
2002;11(3):xix–xxxix. to attention and memory interventions. J Head Trauma Rehabil.
49. Fasotti L, Kovacs F, Eling PATM, Brouwer WH. Time pressure 1996;11:65–78.
management as a compensatory strategy training after closed- 71. Sloan S, Ponsford J. Managing cognitive problems. In: Ponsford
head injury. Neuropsychol Rehabil. 2000;10:47–65. JL, Sloan S, Snow P, eds. Traumatic Brain Injury: Rehabilitation
50. Winkens I, Van Heugten CM, Wade DT, Fasotti L. Training for Everyday Adaptive Living. 2nd ed. London: Psychology Press;
patients in Time Pressure Management, a cognitive strategy for 2012:99–132.
mental slowness. Clin Rehabil. 2009;23(1):79–90. 72. Bayley M, Teasell R, Marshall S, et al. ABIKUS Evidence Based
51. Winkens I, Van Heugten CM, Wade DT, Habets E, Fasotti L. Recommendations for Rehabilitation of Moderate to Severe Acquired
Efficacy of time pressure management in stroke patients with Brain Injury. Toronto, Ontario, Canada: Ontario Neurotrauma
slowed information processing: a randomized controlled trial. Foundation; 2007.
Arch Phys Med Rehabil. 2009;90(10):1672–1679. 73. Wood RL. Rehabilitation of patients with disorders of attention.
52. Cicerone KD. Remediation of ‘working attention’ in mild trau- J Head Trauma Rehabil. 1986;1:43–53.
matic brain injury. Brain Inj. 2002;16(3):185–195. 74. Ben-Yishay Y, Piasetsky EB, Rattock J. A systematic method for
53. Vallat-Azouvi C, Weber T, Leqrand L, Azouvi P. Rehabilitation ameliorating disorders in basic attention. In: Meier MJ, Benton
of the central executive of working memory after severe traumatic AL, Diller L, eds. Neuropsychological Rehabilitation. New York, NY:
brain injury: two single case studies. Brain Inj. 2009;23(6):585– Churchill Livingston; 1987:165–181.
594. 75. Gansler DA, McCaffrey RJ. Remediation of chronic atten-
54. Evans JJ, Greenfield E, Wilson BA, Bateman A. Walking and tion deficits in traumatically brain injured patients. Arch Clin
talking therapy: improving cognitive-motor dual-tasking in neu- Neuropsychol. 1991;6:335–353.
rological illness. J Int Neuropsychol Soc. 2009;15:112–120. 76. Gray JM, Robertson I. Remediation of attentional difficulties
55. Couillet J, Soury S, Leborne C, et al. Rehabilitation of divided following brain injury: three experimental case studies. Brain Inj.
attention after severe traumatic brain injury: a randomised trial. 1989;3:163–170.
Neuropsychol Rehabil. 2010;20(3):321–339. 77. Gray JM, Robertson IH, Pentland B, Anderson SJ.
56. Schmitter-Edgecombe M, Beglinger L. Acquisition of skilled vi- Microcomputer-based cognitive rehabilitation for brain dam-
sual search performance following severe closed-head injury. J Int age. A randomized group controlled trial. Neuropsychol Rehabil.
Neuropsychol Soc. 2001;7(5):615–630. 1992;2:97–116.
57. Meares S, Shores E, Taylor A, et al. Mild traumatic brain in- 78. Malec J, Jones R, Rao N, Stubbs K. Video-game practice effects
jury does not predict acute postconcussion syndrome. J Neurol on sustained attention in patients with cranio-cerebral trauma.
Neurosurg Psychiatry. 2008;79(3):300–306. Cog Rehabil. 1984;2(4):18–23.
58. Mateer CA, Sira CS, O’Connell ME. Putting Humpty Dumpty 79. Niemann H, Ruff RM, Baser CA. Computer-assisted attention
together again. The importance of integrating cognitive and emo- retraining in head-injured individuals: A controlled efficacy study
tional interventions. J Head Trauma Rehabil. 2005;20(1):62–75. of an outpatient program. J Consult Clin Psychol. 1990;58:811–817.
59. Ruff R. Two decades of advances in understanding of mild trau- 80. Novack TA, Caldwell SG, Duke LW, Bergquist TF, Gage RJ. Fo-
matic brain injury. J Head Trauma Rehabil. 2005;20(1):5–18. cused versus unstructured intervention for attention deficits after
60. Wood RL. Understanding the ‘miserable minority’: a diasthesis- traumatic brain injury. J Head Trauma Rehabil. 1996;11(3):52–60.
stress paradigm for postconcussional syndrome. Brain Inj. 81. Park NW, Ingles JL. Effectiveness of attention rehabilitation af-
2004;18(11):1135–1153. ter an acquired brain injury: a meta-analysis. Neuropsychology.
61. Ponsford J. Rehabilitation interventions after mild head injury. 2001;15(2):199–210.
Current Opin Neurol. 2005;18(6):692–697. 82. Park NW, Proulx G, Towers W. Evaluation of the Attention
62. Palmese CA, Raskin SA. The rehabilitation of attention in indi- Process training programme. Neuropsychol Rehabil. 1999;9:135–
viduals with mild traumatic brain injury, using the APT-II pro- 154.
gramme. Brain Inj. 2000;14(6):535–548. 83. Ponsford JL, Kinsella G. Evaluation of a remedial programme
63. Penkam I, Mateer CA. The specificity of attention retraining in for attentional deficits following closed-head injury. J Clin Exp
traumatic brain injury. J Cog Rehabil. 2004;2:13–26. Neuropsychol. 1988;10:693–708.
64. Gould KR, Ponsford JL, Johnston L, Schönberger M. The nature, 84. Robertson I, Gray JM, McKenzie S. Microcomputer-based cog-
frequency and course of psychiatric disorders in the first year nitive rehabilitation of visual neglect: three multiple- baseline
after traumatic brain injury, a prospective study. Psychol Med. single-case studies. Brain Inj. 1988;2:151–163.
2011;41(10):2099–2109. 85. Ruff R, Mahaffey R, Engel J, Farrow C, Cox D, Karzmark P.
65. Bombardier CH, Fann JR, Temkin NR, Esselman PC, Barber J, Efficacy of THINKable in the attention and memory retraining
Dikmen SS. Rates of major depressive disorder and clinical out- of traumatically head-injured patients. Brain Inj. 1994;8(1):3–14.

www.headtraumarehab.com

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
336 JOURNAL OF HEAD TRAUMA REHABILITATION/JULY–AUGUST 2014

86. Sohlberg MM, Mateer CA. Effectiveness of an attention-training lation applied to individually defined goals: a pilot study bridg-
program. J Clin Exp Neuropsychol. 1987;9:117–130. ing theory, assessment, and treatment. J Head Trauma Rehabil.
87. Stablum F, Umilta C, Mogentale C, Carlan M, Guerrini C. Re- 2011;26(5):325–338.
habilitation of executive deficits in closed-head injury and ante- 105. Chen A, Novakovic-Agopian T, Nycum TJ, et al. Training
rior communicating artery aneurysm patients. Psychol Res. 2000; of goal-directed attention regulation enhances control over
63(3–4):265–278. neural processing for individuals with brain injury. Brain.
88. Sturm W, Willmes K, Orgass B, Hartje A. Do specific attention 2011;134(5):1541–1554.
deficits need specific training? Neuropsychol Rehabil. 1997;7:81– 106. Warden DL, Gordon B, McAllister TW, et al. Guidelines for the
193. pharmacologic treatment of neurobehavioral sequelae of trau-
89. Wood RL, Fussey I. Computer-based cognitive retraining: a con- matic brain injury. J Neurotrauma. 2006;23(10):1468–1501.
trolled study. Int Disabil Stud. 1987;9(4):149–153. 107. Leonard BE, McCartan D, White J, King DJ. Methylphenidate:
90. Sohlberg MM, McLaughliin KA, Pavese A, Heidrich A, Pos- a review of its neuropharmacological, neuropsychological and
ner AI. Evaluation of attention process training and brain in- adverse clinical effects. Hum Psychopharmacol. 2004;19(3):151–
jury education in persons with acquired brain injury. J Clin Exp 180.
Neuropsychol. 2000;22:656–676. 108. Arnsten AF, Dudley AG. Methylphenidate improves prefrontal
91. Serino A, Ciaramelli E, DiSantantonio A, Malagu S, Servadei cortical cognitive function through alpha2 adrenoreceptor and
F, Ladavas E. A pilot study for rehabilitation of central execu- dopamine D1 receptor actions: relevance to therapeutic effects
tive deficits after traumatic brain injury. Brain Inj. 2007;21(1): in attention deficit hyperactivity disorder. Behav Brain Funct.
11–19. 2005;1(1):2. doi:10.1186/1744-9081-1181-82.
92. Middleton DK, Lambert MJ, Seggar LB. Neuropsychological re- 109. Willmott C, Ponsford J. Efficacy of methylphenidate in the early
habilitation: microcomputer-assisted treatment of brain-injured rehabilitation of attention following traumatic brain injury: a
adults. Percept Mot Skills. 1991;72:527–530. randomized, crossover, double-blind, placebo controlled trial. J
93. Murray LL, Keeton RJ, Karcher L. Treating attention in mild Neurol Neurosurg Psychiatry. 2009;80(5):552–557.
aphasia: evaluation of attention process training-II. J Commun 110. Whyte H, Hart T, Vaccaro M, et al. Effects of methylphenidate
Disord. 2006;39:37–61. on attention deficits after traumatic brain injury: a multidi-
94. Pero S, Incoccia C, Caracciolo B, Zoccolotti P, Formisano mensional randomized, controlled trial. Am J Phys Med Rehabil.
R. Rehabilitation of attention in two patients with traumatic 2004;83(6):401–420.
brain injury by means of ‘attention process training’. Brain Inj. 111. Kim Y, Ko M, Na S, Park S, Kim K. Effects of single-dose
2006;20(11):1207–1219. methylphenidate on cognitive performance in patients with trau-
95. Zickefoose S, Hux K, Brown J, Wulf K. Let the games begin: matic brain injury: a double-blind placebo-controlled trial. Clin
a preliminary study using Attention Process training -3 and Rehabil. 2006;20:24–30.
Lumosity brain games to remediate attention deficits following 112. Whyte J, Hart T, Schuster K, Fleming M, Polansky M, Coslett
traumatic brain injury. Brain Inj. 2013;27(6):707–716. HB. Effects of methylphenidate on attentional function after
96. Rohling ML, Beverly B, Faust ME, Demakis G. Effectiveness of traumatic brain injury: a randomized placebo-controlled trial.
cognitive rehabilitation following acquired brain injury: a meta- Am J Phys Med Rehabil. 1997;76(6):440–450.
analytic re-examination of Cicerone et al.’s (2000, 2005) system- 113. Plenger PM, Dixon CE, Castillo RM, Frankowski RF, Yablon
atic reviews. Neuropsychology. 2009;23(1):20–39. SA, Levin HS. Subacute methylphenidate for moderate to mod-
97. Dirette DK, Hinojosa J. The effects of a compensatory interven- erately severe traumatic brain injury: a preliminary double-blind
tion on processing deficits of adults with acquired brain injuries. placebo-controlled study. Arch Phys Med Rehabil. 1996;77:536–
Occup Ther J Res. 1999;19(4):223–240. 540.
98. Manly T, Hawkins K, Evans J, Woldt K, Robertson IH. Re- 114. Gualtieri CT, Evans RW. Stimulant treatment for the neu-
habilitation of executive function: facilitation of effective goal robehavioral sequelae of traumatic brain injury. Brain Inj.
management on complex tasks using periodic auditory alerts. 1988;2(4):273–290.
Neuropsychology. 2002;40:271–281. 115. Speech TJ, Rao SM, Osmon DT, Sperry LT. A double-blind
99. Sweeney S, Kersel DA, Morris RG, Manly T, Evans JJ. The sensi- controlled study of methylphenidate treatment in closed-head
tivity of a virtual reality task to planning and prospective memory injury. Brain Inj. 1993;7(4):333–338.
impairments: group differences and the efficacy of periodic alerts 116. Kaelin DL, Cifu DX, Matthies B. Methylphenidate effect on
on performance. Neuropsychol Rehabil. 2010;20(2):239–263. attention deficit in the acutely brain-injured adult. Arch Phys Med
100. Tate R KM, Ponsford J, Douglas J, Velikonka D, Bayley M, Rehabil. 1996;77:6–9.
Stergiou-Kita M, On Behalf of the InCog Expert Panel. INCOG 117. Pavlovskaya M, Hochstein H, Keren O, Mordvinov E,
guidelines for cognitive rehabilitation following traumatic brain Grosswasser Z. Methylphenidate effect on hemispheric atten-
injury: executive functioning and self-awareness. J Head Trauma tional imbalance in patients with traumatic brain injury: a psy-
Rehabil. 2014;29(4):338–352. chophysical study. Brain Inj. 2007;21(5):489–497.
101. McMillan T, Robertson IH, Brock D, Chorlton L. Brief 118. Bleiberg J, Garmoe W, Cederquist J, Reeves D, Lux W. Effects of
mindfulness training for attentional problems after traumatic Dexedrine on performance consistency following brain injury: a
brain injury: A randomised control treatment trial. Neuropsychol double-blind placebo cross-over study. Neuropsychi, Neuropsychol
Rehabil. 2002;12(2):117–125. Behav Neurol. 1993;6(4):245–248.
102. Wilson C, Robertson IH. A home-based intervention for atten- 119. Giacino J, Whyte J, Bagiella E, et al. Placebo-controlled trial of
tional slips during reading following head injury: a single case amantadine for severe traumatic brain injury. New Eng J Med.
study. Neuropsychol Rehabil. 1992;2:193–205. 2012;366(9):819–826.
103. Webster JS, Scott RR. The effects of self-instructional training 120. Kraus MF, Maki P. The combined use of l-dopa/carbidopa in
on attentional deficits following head injury. Clin Neuropsychol. the treatment of chronic brain injury. Brain Inj. 1997;11(6):
1983;5(2):69–74. 455–460.
104. Novakovic-Agopian T, Chen AJ, Rome S, et al. Rehabilita- 121. Kraus MF, Smith GS, Butters M, et al. Effects of the dopamin-
tion of executive functioning with training in attention regu- ergic agent and NMDA receptor antagonist amantadine on

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
INCOG Recommendations for Management of Cognition Following TBI 337

cognitive function, cerebral glucose metabolism and D2 recep- 123. Schneider WM, Drew-Cates J, Wong TM, Dombovy ML. Cog-
tor availability in chronic traumatic brain injury: a study us- nitive and behavioral efficacy of amantadine in acute traumatic
ing positive emission tomography (PET). Brain Inj. 2005;19(7): brain injury: an initial double-blind placebo controlled study.
471–479. Brain Inj. 1999;13(11):863–872.
122. Nickels JL, Schneider WN, Dombovy ML, Wong TM. Clini- 124. Hart T, Whyte J, Ellis C, Chervoneva I. Construct validity of an
cal use of amantadine in brain injury rehabilitation. Brain Inj. attention rating scale for traumatic brain injury. Neuropsychology.
1994;8(8):709–718. 2009;23(6):729–735.

www.headtraumarehab.com

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

You might also like