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# Update on the Efficacy of Cognitive
Rehabilitation After Moderate to Severe
Traumatic Brain Injury: A Scoping Review

Adeline Julien, MSc,ª,ᵇ Lola Danet, PhD,ª,ᵇ Mallaury Loisel, MSc,ᵇ David Brauge, MD,ᵇ,ᶜ
Jérémie Pariente, MD, PhD,ª,ᵇ Patrice Péran, PhD,ᵇ Mélanie Planton, PhDª,ᵇ

From the ªDepartment of Neurology, Toulouse University Hospital, Toulouse, France; ᵇToulouse Neuroimaging Center, Université de Toulouse, Inserm, UPS, Toulouse, France; and ᶜUniversity Sports Clinic, Toulouse University Hospital, Toulouse, France.

**Abstract**

**Objectives:** To identify, categorize, and analyze the methodological issues of cognitive rehabilitation of patients with moderate to severe traumatic brain injury and its efficacy.

**Data Sources:** Pubmed and PsycINFO were searched for studies published between 2015 and 2021 using keywords for cognitive intervention and traumatic brain injury.

**Study Selection:** Two independent reviewers selected articles concerning cognitive rehabilitation for adults with traumatic brain injury. Of 458 studies, 97 full-text articles were assessed and 46 met the inclusion criteria.

**Data Extraction:** Data were analyzed by 1 reviewer according to criteria concerning the methodological quality of studies.

**Data Synthesis:** Results showed a large scope of 7 cognitive domains targeted by interventions, delivered mostly in individual sessions (83%) with an integrative cognitive approach (48%). Neuroimaging tools as a measure of outcome remained scarce, featuring in only 20% of studies. Forty-three studies reported significant effects of cognitive rehabilitation, among which 7 fulfilled a high methodological level of evidence.

**Conclusions:** Advances and shortcomings in cognitive rehabilitation have both been highlighted and led us to develop methodological key points for future studies. The choice of outcome measures, the selection of control interventions, and the use of combined rehabilitation should be investigated in further studies.

Archives of Physical Medicine and Rehabilitation 2023;104:315–30

© 2022 by the American Congress of Rehabilitation Medicine. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/)

Cognitive disorders after a traumatic brain injury (TBI) have been well described in recent decades. Long-term memory, attention, processing speed, executive functions, and self-awareness disorders are frequent and related to the high frequency of temporal and frontal lesions.¹ Cognitive sequelae commonly persist several years after a moderate to severe TBI,²,³ affecting vocational integration and quality of life.⁴,⁵ Cognitive rehabilitation aims to decrease acquired neurocognitive impairment and disability using various and complementary approaches.⁶ Interventions could aim to train or strengthen impaired cognitive functions and/or to implement compensatory mechanisms in addition to external aids.⁶ Metacognitive strategies are also trained in order to facilitate the transfer to different environmental contexts.⁷,⁹

In recent years, the literature has provided quantitative data about cognitive rehabilitation after TBI, leading to a better understanding of the underlying cerebral mechanisms and the development of new interventions. Results were reported across reviews, systematic reviews, meta-analyses, and scoping reviews. The most consequent systematic review was conducted by the Cognitive Rehabilitation Task Force of the American Congress of Rehabilitation Medicine.¹⁰ Since 2000, Cicerone et al have published 4 successive systematic reviews on the cognitive rehabilitation of patients with TBI or stroke and established evidence-based clinical recommendations.⁶,¹⁰⁻¹² Four hundred ninety-one studies have now been reviewed and classified according to the level of evidence, including 109 studies in class I, 68 in class II, and 314 in class III. For each cognitive domain, Cicerone et al¹⁰ provided several levels of recommendations: practice standards, practice guidelines, and practice options. Practice standards, derived from

<footnote>Disclosures: Jérémie Pariente is on the Scientific Board of Biogen. The other authors have nothing to disclose.</footnote>
the strongest evidence, have been identified for treatment of attention deficits, left visual neglect, apraxia, mild memory impairments, language and social communication deficits, mild to moderate executive functions deficits, and holistic neuropsychological rehabilitation. They concluded that future research could investigate the effect of individual characteristics, especially the role of psychological insight, residual cognitive reserve, and the presence of associated psychiatric comorbidities. They also recommended including the frequency and intensity of cognitive rehabilitation as covariates in statistical models. Furthermore, several scoping reviews addressed complementary aspects of TBI, such as societal dimensions,¹³⁻¹⁵ neurologic and neuropsychological patterns,¹⁶⁻¹⁸ psychological conditions associated with TBI,¹⁹ delivery mode of rehabilitation,²⁰,²¹ and state of scientific research on clinical rehabilitation.²²,²³ Two scoping reviews have reported the effects of cognitive rehabilitation²⁴,²⁵ on 2 very specific approaches that focused on driving rehabilitation²⁵ and the use of repeated transcranial magnetic stimulation on cognitive functioning.²⁴

The literature about cognitive rehabilitation after TBI is vast. Reviews on this subject usually analyze the content of rehabilitation to derive recommendations for clinical practice. Here, we chose to focus on methodological criteria to determine the level of scientific evidence of these studies. The most recent substantial systematic review on this subject includes published articles up to 2014.¹⁰ In this article, we aimed to review the scope of interventions in cognitive rehabilitation since 2015. Moreover, we chose to select studies including only patients with TBI and to exclude the stroke population in order to limit the heterogeneity of the underlying physiopathology of cognitive disorders. We also excluded the population with mild TBI because the functional and cognitive outcomes differ from those of moderate to severe TBI.²⁶ Scoping review was an appropriate approach to map the scope and nature of research in cognitive rehabilitation after TBI, summarize research findings, and identify gaps in the existing literature. In order to guide our search, we addressed 4 main questions: (1) Which cognitive domains does cognitive rehabilitation focus on? (2) What are the characteristics of interventions in cognitive rehabilitation? (3) What are the outcome measures used by authors? (4) What is the efficacy of cognitive rehabilitation?

## Methods

The scoping review was based on the framework developed by Arksey and O'Malley²⁷ including the successive stages described below.

### Search strategy

A systematic search of publications listed in the Pubmed (via Medline) and PsycINFO databases was conducted in August 2021

using the keywords “cognitive rehabilitation” (OR “cognitive remediation,” “cognitive intervention,” “cognitive training,” “cognitive treatment”) AND “traumatic brain injury.” The following terms were excluded from the systematic search: “children,” “pediatric,” “concussion,” “mild,” and “animal.” The scope of the search went from January 1, 2015, to July 31, 2021.

## Inclusion and exclusion criteria

Inclusion criteria were as follows: (1) studies including adults or adolescents, no younger than 15 years old, with moderate to severe TBI. The Mayo Classification System criteria were used to define moderate to severe TBI: loss of consciousness lasting 30 minutes or more and/or posttraumatic anterograde amnesia lasting 24 hours or more and/or worst Glasgow Coma Scale score less than 13 in the first 24 hours and/or imaging evidence of intracranial pathology (intracerebral hematoma, subarachnoid hemorrhage, cerebral contusion, etc).²⁸ We also reported for each article whether brain lesions were identified by authors through computed tomography/ magnetic resonance scanning (table 1). In a context of mixed samples including several acquired brain injuries, moderate to severe TBI should be the most represented group. (2) Patients had to be included at least 3 months after the onset. (3) Interventions had to investigate the rehabilitation of cognitive functions. (4) Effects of cognitive rehabilitation had to be documented by quantitative or qualitative comparisons throughout follow-up. (5) Interventions had to be conducted in a rehabilitation center, through ambulatory care, or at home.

Reviews and study protocols were excluded from this research, as were those not written in the English language. Then, for all citations, 2 authors (AJ, ML) conducted an abstract review and excluded articles that did not meet the eligibility criteria. All remaining citations underwent a full-text review.

## Data analysis

For each of the 4 research questions, criteria of analysis were defined and collected in order to classify the characteristics and level of evidence of the reviewed studies.

### Cognitive domains targeted by cognitive rehabilitation

All cognitive functions targeted by rehabilitation were listed. When several cognitive functions were trained, we registered all of them. We consider interventions to be “global training” interventions when they focused on 3 or more cognitive functions or when the aim was defined with the generic term “cognitive skills.”

### Characteristics of cognitive rehabilitation

Types of cognitive rehabilitation were divided into 3 categories of interventions. *Cognitive training* was defined as repetitive exercises without any explicit mention of metacognitive strategy training. *Integrative cognitive intervention* referred to interventions that explicitly combined the training of cognitive functions and metacognitive strategies. Finally, *external aids training* corresponded to the use of external compensatory mechanisms such as notebooks, cell phone applications, and alarms.

We also identified *combined approaches*, which referred to cognitive rehabilitation associated with other interventions like pharmacotherapy or noninvasive brain stimulation.

Three other parameters of cognitive interventions were analyzed: the delivery mode including group vs individual sessions, the length, and the intensity. Length was studied by distinguishing

**List of abbreviations:**

EEG electroencephalography

fMRI functional magnetic resonance imaging

GMT goal management training

TBI traumatic brain injury

tDCS transcranial direct current stimulation

WM working memory
<table><caption>**Table 1** Summary of reviewed studies on cognitive rehabilitation posttraumatic brain injury</caption><thead><tr><th>Authors and Level of Evidence</th><th>Participants*</th><th>Cognitive Rehabilitation Characteristics¹</th><th>Design</th><th>Intervention Characteristics</th><th>Neuropsychological Outcome Measures</th><th>Significant Main Results</th></tr></thead><tbody><tr><td>Cho and Sohlberg²⁹<br>Class III</td><td>3 TBI, including 2 severe TBI<br>Ages: 24, 51, and 52 y</td><td>60 min<br>1 per wk<br>Over 6 wk<br>Total of 6 sessions</td><td>Intra-individual comparison:<br>help-seeking scores before vs<br>after CR</td><td>Group sessions<br>NICE training protocol:<br>Intervention protocol targeting<br>help-seeking behaviors during<br>wayfinding</td><td>Ecological executive assessment<br>(executive function route-finding<br>task)<br>Structured role-plays with a<br>4-point social behavior rating<br>scale</td><td>Absence of statistical analysis<br>Improvements for all 3 patients of<br>ecological measures and<br>structured role-plays</td></tr><tr><td>Constantinidou³⁰<br>Class II</td><td>15 moderate to severe TBI<br>Age: 28.13 (9.21)</td><td>60 min<br>2 to 4 per wk<br>10-12 wk<br>Average total of 27 sessions</td><td>Intergroup comparison:<br>CP training in young adults with<br>TBI vs CP training in young<br>healthy adults vs CP training in<br>older adults vs no training in<br>healthy older adults</td><td>Individual sessions<br>CP training</td><td>Two categorization tests designed<br>for this study<br>Scores on executive function,<br>visuospatial, memory, working<br>memory, and language tests</td><td>Improvement in CP for all treated<br>groups<br>No intergroup differences</td></tr><tr><td>Elbogen et al³¹<br>Class I</td><td>112 TBI with PTSD, including 57%<br>moderate to severe TBI<br>Age: 36.52 (8.42)</td><td>60-90 min<br>3 home visits at 0, 2, 4 mo<br>Over 6 mo</td><td>Intergroup comparison: CR with a<br>CALM vs active control<br>intervention including<br>psychoeducation</td><td>Individual sessions<br>CALM: Goal management training<br>plus mobile devices and<br>attentional control</td><td>Scores on executive functions<br>tests<br>Emotional and behavioral<br>questionnaires<br>Experimental tasks: Multistep<br>everyday tasks</td><td>No improvement on executive<br>performance<br>Improvement on behavioral,<br>emotional, and PTSD symptoms</td></tr><tr><td>Emmanouel et al³²<br>Class I</td><td>18 patients with brain injury,<br>including 11 moderate to<br>severe TBI¹<br>Severity: Period of loss of<br>consciousness ranging<br>from 12 to 33 d<br>Age: 35 (9)</td><td>30 minutes<br>3 to 4 per wk<br>Total of 11 sessions</td><td>Intergroup comparison: CR<br>combining GMT+WM training vs<br>control intervention including<br>GMT only</td><td>Individual sessions<br>BMT combined with WM training</td><td>Scores on executive function,<br>memory, working memory, and<br>language tests<br>Executive ecological assessment.<br>Executive functioning<br>questionnaires (self- and<br>relative-reports).</td><td>Improvements on multistep<br>everyday tasks for the<br>intervention group compared to<br>the control group (medium to<br>large effect sizes)<br>No interaction effects between<br>treatment and time for all other<br>neuropsychological measures</td></tr><tr><td>Goodwin et al³³<br>Class III</td><td>66 patients with ABI, including<br>50 traumatic injuries (46 closed<br>head injuries and 4 open head<br>injuries)<br>Age: 31.6 (11.75)</td><td>Intensive phase: 4 full d/wk<br>Over 12 wk<br>Reintegration phase: 2 or 3<br>full d/wk<br>Over 12 wk<br>Total of 24 sessions</td><td>Intra-individual comparison:<br>Dysexecutive scores before vs<br>after CR</td><td>Individual and group sessions<br>Holistic neuropsychological<br>rehabilitation including 2<br>phases:<br>Intensive phase: education,<br>practical tasks, facilitated<br>discussion, and homework<br>Reintegration phase</td><td>Executive functioning and<br>behavioral questionnaire<br>(self- and relative reports)</td><td>Lower number of self-reported and<br>relative-reported dysexecutive<br>symptoms</td></tr><tr><td>Gracey et al³⁴<br>Class I</td><td>59 acquired nonprogressive brain<br>injuries, including 27 patients<br>with TBI<br>Severity obtained for 55% of<br>participants with TBI: 41%<br>severe, 7% moderate, 7% mild<br>Age: Detailed for each group, not<br>for total sample<br>Min mean age: 47.79 (14.72)<br>Max mean age: 49.76 (12.94)</td><td>90 to 120 min<br>Total number of sessions<br>varied depending on the<br>abilities of the participant</td><td>Longitudinal intergroup<br>comparison<br>Crossover design: Assisted<br>intention monitoring vs control<br>intervention (information and<br>games)</td><td>Individual sessions<br>AIM: Brief GMT combined with<br>periodic SMS text messages</td><td>Proportion of daily intentions<br>achieved by participant</td><td>Improvement of achievement<br>intentions after the<br>intervention phase compared to<br>the control condition (medium<br>effect sizes)</td></tr><tr><td>Hart and Vaccaro³⁵<br>Class I</td><td>8 moderate to severe TBI<br>Age: 23.8 (4.3)</td><td>8 wk<br>No more details</td><td>Intergroup comparison: Goal<br>intention intervention (with<br>text messaging) vs active<br>control group (who received<br>unspecific text messages)</td><td>Individual sessions<br>Goal intention intervention:<br>Implementation of intentions<br>with reminder messages</td><td>Assessment of emotional<br>function, social participation,<br>and goal attainment scaling<br>scores</td><td>Improvement for the<br>experimental group on self- and<br>relative reports for social<br>participation and social<br>relation compared to control<br>group (medium to large effect<br>sizes)</td></tr></tbody><tfoot><tr><td colspan="7" style="text-align: right;">(continued on next page)</td></tr></tfoot></table>
<table><tbody><tr><td>Powell et al<sup>36</sup><br>Class I</td><td>23 ABI (including 14 motor vehicle collisions, 1 fall, and 2 assaults)<br>No information regarding severity<br>Age: 44 (15)</td><td>60 min<br>Over 8 wk<br>Total of 6 sessions</td><td>Intra-individual comparison:<br>problem solving, self-efficacy,<br>and life satisfaction self-report<br>scores before vs after CR</td><td>Individual sessions<br>Implementation of web-based<br>program (Prosolv program) for<br>problem solving in daily life</td><td>Self-report questionnaires on<br>problem solving, self-efficacy,<br>and life satisfaction scores</td><td>No difference</td></tr><tr><td>Siponkoski et al<sup>37</sup><br>Class I</td><td>40 moderate to severe TBI<br>Age: 41.3 (13.3)</td><td>60 min<br>2 times per wk<br>Over 3 mo<br>Total of 20 sessions</td><td>Longitudinal intergroup<br>comparison<br>Crossover design: intervention<br>phase vs control phase<br>(standard care)</td><td>Individual sessions<br>Neurological music therapy:<br>intervention adapted from 2<br>existing music therapies<br>(functionally oriented music<br>therapy and music-supported<br>training)</td><td>Scores on executive function,<br>memory, attention, and<br>reasoning tests</td><td>Improvement of cognitive<br>functioning in the AB group<br>(ie, intervention phase<br>followed by control phase)<br>Increase in gray matter volume<br>(right inferior frontal gyrus) in<br>both groups during<br>intervention and control<br>periods<br>No difference on frontal gray<br>matter volume after training<br>Significant negative correlation<br>between changes in processing<br>speed score and gray matter<br>volume of putamen area</td></tr><tr><td>Vander Linden et al<sup>38</sup><br>Class III</td><td>16 moderate to severe TBI<sup>†</sup><br>Age: 15 y 8 mo (1 y 7 mo)</td><td>40 min<br>5 per wk<br>Over 8 wk<br>Total of 40 sessions</td><td>Intergroup comparison: changes<br>in gray matter volume in<br>regions of interest related to<br>executive functions after<br>cognitive training vs changes<br>in gray matter volume in<br>control regions</td><td>Individual sessions<br>Brain games software: Home-<br>based cognitive training<br>program targeting executive<br>functions and attention</td><td>Scores on working memory,<br>executive function, attention,<br>and processing speed tests</td><td>At 6-mo follow-up, lower effect<br>from training on executive<br>functions was found in<br>adolescents with diffuse axonal<br>injuries in the deep brain nuclei<br>compared to adolescents<br>without diffuse axonal injuries<br>in this area</td></tr><tr><td>Vander Linden et al<sup>39</sup><br>Class II</td><td>16 moderate to severe TBI<sup>†</sup><br>Age: 15 y 8 mo (1 y 7 mo)</td><td>40 min<br>5 per wk<br>Over 8 wk<br>Total of 40 sessions</td><td>Intergroup comparison:<br>computerized cognitive<br>training vs healthy control<br>group (no training)</td><td>Individual sessions<br>Brain games software: Home-<br>based cognitive training<br>program targeting executive<br>functions and attention</td><td>Scores on working memory,<br>executive functions, attention,<br>and processing speed tests<br>Executive functioning and<br>behavioral questionnaires<br>(relative report)</td><td>Small to large effect size of<br>intervention on all<br>neuropsychological measures<br>Results maintained or increased at<br>6-mo follow-up</td></tr><tr><td>Verhelst et al<sup>40</sup><br>Class III</td><td>5 moderate to severe TBIs<sup>†</sup><br>Age: 16 y (9 mo)</td><td>40 min<br>5 per wk<br>Over 8 wk<br>Total of 40 sessions</td><td>Intra-individual comparison:<br>executive performance before<br>and after CR</td><td>Individual sessions<br>Brain games software: Home-<br>based cognitive training<br>program targeting executive<br>functions and attention</td><td>Scores on attention, working<br>memory, and executive<br>function tests<br>Executive functioning and<br>behavioral questionnaires (self-<br>and relative reports)</td><td>Time × Group interaction effects<br>on 1 attention score and on 1<br>executive function score (small<br>to moderate effect sizes)</td></tr><tr><td>Verhelst et al<sup>41</sup><br>Class II</td><td>16 moderate to severe TBIs<sup>†</sup><br>Age: 15 y (1.8)</td><td>40 min<br>5 per wk<br>Over 8 wk<br>Total of 40 sessions</td><td>Intergroup comparison: white<br>matter changes in TBI group vs<br>healthy control group</td><td>Individual sessions<br>Brain games software: Home-<br>based cognitive training<br>program targeting executive<br>functions and attention</td><td>Scores on attention, working<br>memory, and executive<br>function tests<br>Executive functioning and<br>behavioral questionnaires (self-<br>and relative reports)</td><td>Time × Group interaction effects<br>on 1 attention score and on 1<br>executive function score (small<br>to moderate effect sizes)</td></tr><tr><td colspan="7"><strong>Attention</strong></td></tr><tr><td>Arroyo-Ferrer et al<sup>42</sup><br>Class III</td><td>20-year-old man with TBI<sup>†</sup><br>Axonal damage was diagnosed<br>using MRI</td><td>45 min<br>4 sessions per wk<br>Over 6 wk<br>Total of 16 sessions</td><td>Case report</td><td>Individual sessions<br>EEG-based NFB intervention<br>targeting inhibition of theta<br>frequency band in frontal areas<br>during exercises in virtual<br>environments<br>Neuropsychological intervention<br>aiming attention, executive<br>function, and working memory</td><td>Scores on executive function,<br>memory, attention, and<br>visuospatial ability tests</td><td>Improvement of visuospatial<br>abilities, attention, and<br>executive function after EEG-<br>based NFB intervention<br>compared to after<br>neuropsychological<br>intervention<br>Correlative quantitative EEG<br>changes were found</td></tr><tr><td>Dundon et al<sup>43</sup><br>Class I</td><td>26 TBI<br>Information regarding regions of</td><td>Not detailed</td><td>Intergroup comparison: adaptive<br>training group vs nonadaptive</td><td>Individual sessions<br>Dichotic listening training task</td><td>Scores on attention and memory<br>tests</td><td>Improvement with both trainings<br>on cognitive variables</td></tr></tbody><tfoot><tr><td colspan="7">(continued on next page)</td></tr></tfoot></table>
<table><tbody><tr><td>Dymowski et al<sup>44</sup><br>Class II</td><td>damage for 23/26 participants<br>Age: 37.3 (9.98)<br>3 severe TBI<sup>†</sup><br>Ages: 21, 27, and 53</td><td>60 min<br>2-3 per wk<br>Over 12 to 16 wk<br>Total of 9 sessions</td><td>training group vs no training<br>control group<br>Single-case design repeated<br>across subjects: baseline phase<br>vs attention training phase and<br>attention training phase vs<br>individualized strategies<br>training phase</td><td>Individual sessions<br>Computerized attention training:<br>APT-3</td><td>Self-report questionnaires of<br>global cognitive disorders<br>Scores on processing speed and<br>attention tests.<br>Questionnaire of attentional<br>complaint (self- and relative<br>reports)</td><td>Interaction between group and<br>time was not significant<br>Improvement in speed processing<br>scores after attentional training<br>and strategy learning</td></tr><tr><td>Fitzgerald et al<sup>45</sup><br>Class I</td><td>11 moderate to severe TBI<sup>†</sup><br>Age: Detailed for each group, not<br>for total sample<br>Min mean age: 27.2 (5.6)<br>Max mean age: 33.78 (13.33)</td><td>40 min<br>2 per wk<br>Over 4 wk<br>Total of 8 sessions</td><td>Intergroup comparison: error<br>awareness training vs no<br>feedback group</td><td>Individual sessions<br>Computer-based intervention<br>program for improving error<br>awareness: participants<br>received feedback on errors</td><td>Specific task about error<br>awareness<br>Scores on global functioning,<br>executive function, and<br>attention tests<br>Self- and relative reports on<br>dysexecutive questionnaires<br>Scores on memory, attention,<br>executive function, and<br>processing speed tests</td><td>Improvement of error awareness<br>scores (large effect size in the<br>experimental group)<br>No change in group who did not<br>receive feedback</td></tr><tr><td>McDonald et al<sup>46</sup><br>Class I</td><td>72 TBI: 36 mild, 8 complicated<br>mild, 8 moderate, 23 severe<br>Age: Detailed for each group, not<br>for total sample<br>Min mean age: 37.2 (12.0)<br>Max mean age: 43.1 (12.3)</td><td>50 min<br>2 per wk<br>Over 4 wk<br>Total of 8 sessions</td><td>Intergroup comparison: cognitive<br>behavioral therapy vs repetitive<br>cognitive tasks combined with<br>methylphenidate or placebo</td><td>Individual sessions<br>MAAT: metacognitive intervention<br>ABT: Repetitive cognitive tasks</td><td>Scores on visuospatial, semantic<br>fluency, divided attention,<br>working memory, and long-term<br>memory tests</td><td>Improvement in scores for<br>learning, working memory, and<br>divided attention after<br>combined MAAT/<br>methylphenidate intervention<br>Better memory improvement<br>scores after MAAT compared to<br>ABT intervention</td></tr><tr><td>Sacco et al<sup>47</sup><br>Class I</td><td>32 severe TBI<br>Age: 37.7 (10.4)</td><td>60 min (including 20 min<br>tDCS+40 min cognitive<br>rehabilitation)<br>Twice per d<br>Over 5 d<br>Total of 10 sessions</td><td>Intergroup comparison: real tDCS<br>group vs placebo tDCS group</td><td>Individual sessions<br>Computerized rehabilitation of<br>divided attention combined<br>with unilateral or bilateral tDCS<br>on dorsolateral prefrontal<br>cortex (depending on the<br>hemispheric lesion distribution<br>for each patient), 20 min 2 mA<br>Group sessions<br>Sessions combined “Medal of<br>Honor: Rising Sun” games on<br>PlayStation 2 (first-person<br>shooter action video game) and<br>psychoeducation program with<br>compensatory strategies</td><td>Scores on visuospatial, semantic<br>fluency, divided attention,<br>working memory, and long-term<br>memory tests</td><td>Improvement in divided attention<br>score in experimental group<br>No change over the pretreatment<br>phase and within the control<br>group<br>Reorganization of neuronal<br>activations on fMRI</td></tr><tr><td>Vakili et al<sup>48</sup><br>Class I</td><td>31 TBI<br>Average length of posttraumatic<br>amnesia (d): intervention<br>group: 41.87 (43.87); control<br>group: 43.64 (35.64)<br>Age: Detailed for each group, not<br>for total sample<br>Min mean age: 27.73 (11.43)<br>Max mean age: 28.63 (6.54)</td><td>2 h<br>Once a wk<br>Over 8 wk<br>Total of 8 sessions</td><td>Intergroup comparison: video<br>games group vs passive control<br>group (usual care)</td><td>Game performance on PlayStation<br>2<br>Attentional blink task<br>Scores on attention tests<br>Self-report questionnaires of<br>quality of life, self-efficacy, and<br>executive functioning</td><td>Improvements in game<br>performance, attentional blink,<br>and attentional task, implying<br>processing speed<br>No change in behavioral and self-<br>efficacy scales scores</td><td></td></tr><tr><td>Jones et al<sup>49</sup><br>Class I</td><td>15 ABI, including 9 moderate to<br>severe TBI<br>Age: Detailed for each group, not<br>for total sample<br>Min mean age: 51.9 (11.02)<br>Max mean age: 55.4 (10.54)</td><td>45 min<br>1 session per wk<br>Over 3 wk<br>Total of 3 sessions</td><td>Intergroup comparison: MACT vs<br>APT</td><td>Individual sessions<br>MACT: Structured music-based<br>auditory training exercises to<br>practice attention functions<br>APT: Computer-based tasks to<br>address focused, sustained,<br>selective, alternating, and<br>divided attention</td><td>Scores on attention and executive<br>tests</td><td>Improvements in 1 of the 3<br>attention and executive tests<br>(TMT B) after the intervention<br>for the MACT group compared to<br>the APT group</td></tr><tr><td colspan="7"><strong>Memory</strong></td></tr><tr><td>Chiaravalloti et al<sup>50</sup><br>Class I</td><td>18 TBI: 3 mild, 3 moderate, 12<br>severe<br>Age: Detailed for each group, not<br>for total sample</td><td>45 to 60 min<br>Twice per wk<br>Over 5 wk<br>Total 10 sessions</td><td>Intergroup comparison: treatment<br>group vs placebo control group<br>(memory exercises but not</td><td>Individual sessions<br>Modified story memory technique,<br>involving the training of<br>mental imagery and the use of</td><td>BOLD signal on fMRI, word<br>learning task, and word<br>recognition task<br>Scores on memory tests</td><td>Improvement in prose recall<br>compared to placebo group<br>fMRI: Changes in activation in<br>executive control network and<br>(continued on next page)</td></tr></tbody></table>
<table><tbody><tr><td>Chiaravallotti et al<sup>51</sup><br>Class I</td><td>Min mean age: 42.22 (14.12)<br>Max mean age: 45.78 (10.53)<br>69 moderate to severe TBI<br>Age: Detailed for each group, not<br>for total sample<br>Min mean age: 37.17 (11.24)<br>Max mean age: 40.68 (11.28)</td><td>45 to 60 min<br>Twice per wk<br>Over 5 wk<br>Total 10 sessions</td><td>exposed to critical components<br>of training)<br>Intergroup comparison: treatment<br>group vs placebo control group<br>(non-training-oriented tasks)</td><td>the source/context of learned<br>information<br>Individual sessions<br>Modified story memory technique,<br>involving the training of<br>mental imagery and the use of<br>the source/context of learned<br>information</td><td>Scores on memory tests<br>Ecological scores on the<br>Rivermead Behavioural Memory<br>Test<br>Cognitive and behavioral<br>executive questionnaires (self-<br>and relative reports)</td><td>default mode network<br>(Bonnerroni correction)<br>Improvement in prose recall<br>compared to placebo group<br>(medium effect size)<br>No treatment effect on<br>standardized memory scores<br>Improvement on Rivermead<br>Behavioural Memory Test in the<br>experimental group compared<br>to placebo group</td></tr><tr><td>Hara et al<sup>52</sup><br>Class III</td><td>67-year-old man who sustained a<br>diffuse axonal injury<sup>‡</sup></td><td>6 per wk<br>Over 2 wk<br>Total of 12 sessions</td><td>Case report</td><td>Individual sessions<br>Repeated transcranial magnetic<br>stimulation (2400 pulses once a<br>d) combined with CR (training<br>program focused on memory<br>and attention disorders)</td><td>Scores on memory, attention, and<br>executive function tests<br>Everyday memory assessment<br>scores on Rivermead<br>Behavioural Memory Test</td><td>Absence of statistical analysis<br>2-point gain on the MMSE</td></tr><tr><td>Leśniak et al<sup>53</sup><br>Class I</td><td>65 ABI including 30 TBIs, 27<br>CVAs, 4 encephalitis<br>Age: Detailed for each group, not<br>for total sample<br>Min mean age: 39.6 (15)<br>Max mean age: 42.2 (14)</td><td>60 min<br>5 per wk<br>Over 3 wk<br>Total 15 sessions</td><td>Intergroup comparison: individual<br>therapy group vs group therapy<br>group vs no therapy group</td><td>Individual and group sessions<br>Increased awareness of memory<br>deficits and learning of global<br>strategies for everyday memory</td><td>Scores on memory tests<br>Ecological memory scores (RBMT)<br>Self-report of everyday memory<br>complaint</td><td>No difference between groups<br>In individual therapy group,<br>significant improvements on<br>computerized memory,<br>attention, and working memory<br>tests<br>In group therapy group, decrease<br>of memory failures in daily life<br>(relative report)<br>Improvement of cognitive scores<br>(small to moderate effect sizes)<br>Improvement on self- and relative<br>report measures<br>Gains maintained at 4-mo follow-<br>up</td></tr><tr><td>Leśniak et al<sup>54</sup><br>Class III</td><td>15 moderate to severe TBI<sup>†</sup><br>Age: 26.2 (7.6)</td><td>5 individual and 5 group<br>sessions per wk<br>Over 3 wk<br>Total of 30 sessions</td><td>Intergroup comparison:<br>comprehensive therapeutic<br>program vs waiting list control<br>condition</td><td>Group and group sessions<br>Group sessions: Internal memory<br>strategy training and<br>implementation of external<br>aids. Discussion about memory<br>problems and their respective<br>compensatory strategies<br>Individual sessions: exercises<br>using memory strategies on<br>Rehacom software</td><td>Scores on episodic memory,<br>working memory, and attention<br>tests<br>Self- and relative reports on<br>cognitive measures</td><td>Improvement of prospective<br>memory measure after active<br>treatment phase only<br>Improvement on self-report<br>questionnaire for everyday<br>memory<br>Improvement maintained at 1-y<br>follow-up for all previous<br>results</td></tr><tr><td>Raskin et al<sup>55</sup><br>Class III</td><td>20 moderate to severe TBI<br>Age: 42.11 (13.21)</td><td>60 min<br>1 or 2 per wk<br>Over 6 mo<br>Total of sessions not specified</td><td>Longitudinal intergroup<br>comparison<br>Crossover design: active treatment<br>condition vs no treatment<br>phase at baseline and at 1-y<br>follow-up</td><td>Individual sessions<br>Metacognitive technique using<br>mental imagery</td><td>Prospective memory scores<br>Scores on attention, retrospective<br>memory, and executive<br>function tests<br>Self-report questionnaires about<br>prospective memory, everyday<br>memory, and quality of life</td><td>Improvement of prospective<br>memory measure after active<br>treatment phase only<br>Improvement on self-report<br>questionnaire for everyday<br>memory<br>Improvement maintained at 1-y<br>follow-up for all previous<br>results</td></tr><tr><td colspan="7"><strong>Global Training</strong></td></tr><tr><td>Buccellato et al<sup>56</sup><br>Class III</td><td>21 ABI, including 62% mild to<br>severe TBI<br>Age: 41 (13.38)</td><td>30 to 40 min<br>3 per wk<br>Over 6 wk<br>Total of 18 sessions</td><td>Longitudinal comparison<br>Crossover within-subjects design:<br>global cognitive training phase<br>with the Brainer Virtual<br>Rehabilitation software vs</td><td>Individual sessions<br>Virtual reality training using<br>Bright Brainer Virtual<br>Rehabilitation software (global<br>cognitive training)</td><td>Scores on sustained attention,<br>processing speed, working<br>memory, and visuospatial tests<br>Neurobehavioral symptoms<br>inventory and mood<br>questionnaire</td><td>No significant difference between<br>phases</td></tr></tbody><tfoot><tr><td colspan="7">(continued on next page)</td></tr></tfoot></table>
<table><thead><tr><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th></tr></thead><tbody><tr><td>De la Rosa-Arredondo et al<sup>57</sup><br>Class III</td><td>26-year-old woman with severe TBI<sup>†</sup></td><td>1 time per wk<br>Over 24 wk<br>Total of 24 sessions</td><td>standard-of-care therapies phase<br>Case report</td><td>Individual sessions<br>CR including 2 phases of 12 wk: phase 1 targeted sustained and selective attention and visuospatial abilities; phase 2 focused on memory and executive functions</td><td>Scores on attention, working memory, memory, visuospatial, and abstract reasoning tests</td><td>Absence of statistical analysis<br>Improvement in selective attention, verbal fluency, visuospatial ability, and executive function scores</td></tr><tr><td>De Luca et al<sup>58</sup><br>Class I</td><td>100 mild to moderate TBI<br>Brain lesion site specified<br>Age: 39.9 (10.1)</td><td>60 min<br>3 times per wk<br>Over 8 wk<br>Total of 24 sessions</td><td>Intergroup comparison:<br>Virtual reality training group vs traditional CR group</td><td>Individual sessions<br>Semi-immersive virtual reality using Nirvana BTS-N software, targeting attention, executive function, and visuospatial training</td><td>Scores on global scale, executive functions, and attention tests</td><td>Improvements on cognitive and mood scores for both traditional and virtual reality training<br>Improvements on cognitive flexibility for virtual reality training</td></tr><tr><td>Eilam-Stock et al<sup>59</sup><br>Class III</td><td>29-year-old man with a moderate TBI</td><td>30 min/d (including initial safety checks and 20 min of tDCS combined with cognitive training)<br>5 times per wk<br>Over 4 wk<br>Total of 20 sessions</td><td>Case report</td><td>Individual sessions<br>Computerized CR with BrainHQ program (attention, processing speed, executive function, and working memory) combined with tDCS (anodal electrode on the left DLPFC and a cathodal electrode on the right DLPFC, 20 min 2 mA)</td><td>Scores on attention, working memory, processing speed, executive function, and memory tests<br>Mood, sleep, pain, and fatigue self-report scales</td><td>Absence of statistical analysis<br>Improvement in several cognitive domains: attention, working memory, processing speed, and semantic fluency<br>Improvement in emotional functioning: mood, sleep, and fatigue</td></tr><tr><td>Hwang et al<sup>60</sup><br>Class I</td><td>96 TBI<br>No classification of severity<br>49% of participants with positive CT scan findings<br>Age: Detailed for each group, not for total sample<br>Min mean age: 65.8 (10.7)<br>Max mean age: 68.1 (11.4)</td><td>Once a wk<br>Over 6 mo<br>Total of sessions not specified</td><td>Intergroup comparison:<br>CCT group or TC group vs usual care group</td><td>Individual sessions<br>Computerized cognitive training using Rehacom software (attention, memory, speed of processing, executive functioning)</td><td>Scores on global cognitive scales and executive function tests</td><td>Improvement on attention, memory scales, and global cognitive scale scores after the intervention for the CCT group compared to usual care<br>No difference at 6-mo follow-up<br>Improvement on conceptualization scores and global cognitive scale for the TC group compared to usual care<br>Differences between CCT and TC were not investigated</td></tr><tr><td>Kanchan et al<sup>61</sup><br>Class II</td><td>10 moderate to severe TBI<br>Age: 20-40</td><td>45 min<br>1 to 5 times per wk<br>Over 6 mo<br>Total of session not specified</td><td>Intergroup comparison: cognitive training vs passive control group (no training)</td><td>Individual sessions<br>Brainwave-R software: cognitive strategies and techniques for brain injury rehabilitation (attention, visual processing, information processing, memory, executive function)</td><td>Scores on cognitive battery (Luria Nebraska Neuropsychological Battery Adults-Form I)</td><td>Improvement for all impaired cognitive areas in the experimental group<br>Differences between experimental group and passive control group after training</td></tr><tr><td>Kumar et al<sup>62</sup><br>Class III</td><td>34-year-old woman with severe TBI<sup>‡</sup></td><td>2 h<br>3 per wk<br>Over 2 mo<br>Total of 18 sessions</td><td>Case report</td><td>Individual sessions<br>Immersive environment (coffeehouse) targeting practice job activities, which involved motor, social, and cognitive skills</td><td>Score on executive function tests<br>Self-report quality of life</td><td>Absence of statistical analysis<br>Improvement on TMT B score after intervention compared to baseline</td></tr><tr><td>Maggio et al<sup>63</sup><br>Class II</td><td>56 TBI<sup>†</sup><br>Information regarding brain</td><td>30 min<br>5 times per wk</td><td>Intergroup comparison:<br>Lokomat training with virtual reality</td><td>Individual sessions<br>Lokomat training with or without virtual reality</td><td>Score on general cognitive status, frontal ability, and attention tests</td><td>Improvements on global cognitive scores, executive, and</td></tr></tbody><tfoot><tr><td colspan="7" style="text-align: center;">(continued on next page)</td></tr></tfoot></table>
<table><tr><td>Pinard et al<sup>64</sup><br>Class III</td><td>lesion sites<br>Age: 35.5 (5.3)<br>3 severe TBI<br>Ages ranged between 39 and 57 y</td><td>Over 8 wk<br>Total of 40 sessions<br>Over 15 mo<br>Length varied for each user<br>Total session not detailed</td><td>reality vs Lokomat without<br>virtual reality<br>Case report</td><td>Individual sessions<br>Implementation and training to use a cognitive assistive technology for meal preparation called COOK (Cognitive Orthosis for coOKing)<br>Individual sessions<br>CR including attention and prospective memory training and metacognitive strategy instructions</td><td>Qualitative scores of numbers of meals prepared per wk with the stove, number of warnings, number of interventions of security modules<br>Scores on executive functions, attention, and communication tests<br>Self-report of quality of life</td><td>attention scores for the experimental group<br>Absence of statistical analysis<br>For 2 of 3 participants, increased number of meals prepared per wk<br>Improvement on executive and attentional scores and quality of life scale<br>Cerebral activation task:<br>Increased activation in middle and inferior frontal gyrus and superior temporal gyrus<br>Resting state: greater functional integration of frontal and parietal cortices, visual, and auditory association areas and portions of the cerebellar vermis<br>Structural (DTI-measured FA; P&lt;.01 uncorrected): increased FA in white matter tracts throughout the brain.<br>Especially in tracts serving the prefrontal, occipito-parietal, and temporal association cortices and cerebellum<br>No difference between the 3 groups</td></tr><tr><td>Välimäki et al<sup>66</sup><br>Class I</td><td>90 TBI<sup>†</sup><br>Severity defined with the presence of intracranial injury and sequelae of injuries to the head (ICD-10)<br>Age: 41</td><td>30 min/d<br>Over 8 wk<br>Total of 8 sessions</td><td>Intergroup comparison:<br>rehabilitation gaming group vs entertainment gaming (PlayStation 3) group vs passive control group (no gaming)</td><td>Individual sessions<br>Rehabilitation gaming with Cognifit software (cognitive training platform with 3 categories of exercises: memory, spatial, and mental planning)<br>Individual sessions<br>Comprehensive multifaced intervention including computer-assisted cognitive impairment rehabilitation system targeting memory, attention, and visuospatial defects</td><td>Scores on processing speed, visuomotor tasks, attention, executive function, and working memory tests<br>Executive self-report questionnaire<br>Score on general cognitive status</td><td>Absence of statistical analysis<br>Global improvement of cognitive performance<br>DTI neuroimaging: number and length of callosal fiber bundle increased, especially for fibers connecting the bilateral hemispheres</td></tr><tr><td>Wu et al<sup>67</sup><br>Class III</td><td>50-year-old man, TBI with multiple contusions and lacerations, diffuse axonal injury, and scattered cerebral hemorrhages<sup>†</sup></td><td>30 min<br>5 times per wk<br>Over 1 mo<br>Total of sessions not specified</td><td>Case report</td><td>Individual sessions and with communication partner<br>CommCope-I program:<br>Communication-specific coping intervention</td><td>Communication specific coping scores<br>Scores on functional communication abilities scale</td><td>Improvements in communication-specific coping strategies<br>scores (moderate to medium effect sizes)<br>Improvements in functional communication scores (moderate effect size)</td></tr><tr><td>Communication<br>Douglas et al<sup>68</sup><br>Class III</td><td>13 severe TBI<br>Age: 35.2 (9.3)</td><td>Twice per wk<br>Over 6 wk<br>Total of 12 sessions</td><td>Intra-individual comparison:<br>communication scores before vs after intervention vs 3-mo follow-up</td><td></td><td></td><td></td></tr></table>

(continued on next page)
<table><thead><tr><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th><th></th></tr></thead><tbody><tr><td>Bosco et al<sup>69</sup><br>Class III</td><td>19 severe TBI<br>Age: 38.5 (10.8)</td><td>1.5 h<br>Twice per wk<br>Over 12 wk<br>Total of 24 sessions</td><td>Longitudinal comparison<br>Crossover within-subjects design: cognitive pragmatic treatment vs unspecific activities phase</td><td>Group sessions<br>Cognitive pragmatic treatment: rehabilitation training program for communicative-pragmatic abilities</td><td>Scores on attention, memory, executive function, and logical reasoning tests<br>Scores on theory of mind test<br>Scores on communicative pragmatic tests<br>Scores on Functional Communication Abilities Scale</td><td>Improvements on stress scores (moderate effect size)<br>Overall improvement in pragmatic scores<br>Scores remained stables at 3-mo follow-up</td><td></td></tr><tr><td>Gabbatore et al<sup>70</sup><br>Class III</td><td>15 severe TBI<sup>‡</sup><br>Age: 36.7 (8.73)</td><td>1.5 h<br>Twice per wk<br>Over 12 wk<br>Total of 24 sessions</td><td>Longitudinal comparison<br>Crossover within-subjects design: cognitive pragmatic treatment vs unspecific activities phase</td><td>Group sessions<br>Cognitive pragmatic treatment: rehabilitation training program for communicative-pragmatic abilities</td><td>Scores on attention, memory, executive function, and language tests<br>Scores on communicative pragmatic tests<br>Scores on theory of mind test</td><td>Improvement in comprehension and production scores<br>Improvement in long-term verbal memory and cognitive flexibility</td><td></td></tr><tr><td>Sacco et al<sup>71</sup><br>Class III</td><td>8 severe TBI<br>Age: 36.37 (8.6)</td><td>1.5 h<br>Twice per wk<br>Over 12 wk<br>Total of 24 sessions</td><td>Longitudinal comparison<br>Crossover within-subjects design: cognitive pragmatic treatment vs unspecific activities phase</td><td>Group sessions<br>Cognitive pragmatic treatment: rehabilitation training program for communicative-pragmatic abilities</td><td>Scores on communicative pragmatic tests</td><td>Improvement in comprehension and production scores</td><td></td></tr><tr><td>Social Cognition<br>Westerhof-Evers et al<sup>72</sup><br>Class I</td><td>61 moderate to severe TBI<br>Age: 43.2 (13)</td><td>60 min<br>1 or 2 per wk<br>Total of 16 to 20 sessions</td><td>Intergroup comparison: social cognition and emotional regulation protocol training vs active control treatment (computerized cognitive training)</td><td>Individual sessions<br>T-ScEmo protocol including 3 modules (enhancing emotion perception, perspective taking and theory of mind, basic and goal-directed social behavior)</td><td>Scores on social cognition tests<br>Scores on attention and executive function tests<br>Self- and relative reports: dysexecutive symptoms, social monitoring, empathy</td><td>Improvement for the experimental group on facial affect recognition, theory of mind compared to the control group<br>Improvement in relative-reported empathic behavior and societal participation</td><td></td></tr><tr><td>Topographic Orientation<br>Boccia et al<sup>73</sup><br>Class III</td><td>49-year-old man with extensive head trauma and a coma (period of 1 wk)<sup>‡</sup></td><td>Over 8 wk<br>No information regarding intensity</td><td>Case report</td><td>Individual session<br>Imagery-based treatment including 2 phases (imagery training in order to rapidly generate mental images, generating and retrieving mental images)</td><td>Scores on working memory, cognitive map test, and 3D mental rotation tests<br>Ecological navigational tasks in real environment</td><td>Improvement of topographic skills and episodic memory scores</td><td></td></tr><tr><td>Verbal Auditory Perception<br>Kim et al<sup>74</sup><br>Class III</td><td>65-year-old patient with TBI<sup>‡</sup><br>Information about lesion area</td><td>Over 2 mo<br>No information regarding intensity</td><td>Case report</td><td>Individual sessions<br>Speech therapy and cognitive rehabilitation (cognitive domains not specified)</td><td>Scores on Global Cognitive Scale and aphasia test</td><td>Improved isolated-word verbal comprehension<br>No change in sentence comprehension</td><td></td></tr></tbody></table>

NOTE. For each study, all cognitive functions targeted by rehabilitation were listed. If several cognitive functions were trained, all were registered, but each study was classified according to the main cognitive function trained.

Abbreviations: ABI, acquired brain injury; ABT, attention builders training; AIM, assisted intention monitoring; APT, attention process training; BOLD, blood oxygen level-dependent; CALM, cognitive application for life management; CCT, computerized cognitive training; CR, cognitive rehabilitation; CT, computed tomography; CVA, cerebral vascular accident; CP, categorization performance; DLPFC, dorsolateral prefrontal cortex; DTI, diffusion tensor imaging; FA, fractional anisotropy; ICD, *International Classification of Diseases*; MAAT, memory and attention adaptation training; MACT, music attention control training; MMSE, Mini Mental State Examination; NFB, neurofeedback; NICE, *Noticing you have a problem, Identifying the information you need for help, Compensatory strategies, Evaluating progress; PTSD, posttraumatic stress disorder; RBMT, rivermead behavioral memory test; SMS, short messaging service; TC, Tai Chi; TMT B, trail making test - part B; T-ScEmo, treatment for impairments in social cognition and emotion regulation.

* Participants: n, TBI severity, mean age in years (SD).

† Cognitive rehabilitation characteristics: Length for each session; intensity (eg, number of cognitive rehabilitation sessions per week and number of weeks), total of sessions.

‡ Brain lesions were identified by authors through computed tomography/magnetic resonance scanning for all included patients.
very short (≤1 week), short (1 week to 1 month), moderate (1-3 months), and high (>3 months) duration. Intensity was classified as low (1 session per week), moderate (2 sessions per week), or high (≥3 sessions per week).

## Behavioral examination and neuroimaging as outcome measures

Concerning behavioral outcome measures, 4 types of assessment were distinguished: (1) neuropsychological examination including standardized neuropsychological tests; (2) ecological neuropsychological examination including standardized tests and/or experimental ecological tasks with reference to daily life situations; (3) self-reporting of cognitive complaints, social participation in everyday activities, and quality of life; (4) relative reporting of patient's difficulties in daily life. We also counted the number of these types of assessment for each study in order to attest to the exhaustiveness of the assessment.

Neuroimaging outcome measures were classified as structural and/or functional imaging and/or electroencephalography (EEG).

## Efficacy of cognitive rehabilitation

The efficacy of cognitive rehabilitation was analyzed according to 3 main criteria and associated subcriteria detailed below. A coding grid was used for the extraction of these methodological criteria.

The outcome measures were the first criteria. We first pointed out the results showing a significant improvement in at least 1 of the outcome measures defined by the authors. Quantitative and qualitative improvements were coded when collected. Second, if a significant and/or clinically relevant change was reported, we distinguished whether it was in the primary or secondary outcome measures.

The internal validity of reviewed studies was assessed as secondary criteria, based on the classification used by Cicerone et al in systematic reviews.⁶ According to this classification, studies were classified as class I when they were well-designed, prospective, randomized controlled trials. Class II referred to prospective, nonrandomized cohort studies, retrospective, nonrandomized case-control studies, or multiple baseline studies that allowed a direct comparison between treatment conditions. Class III included clinical series without concurrent controls or single-subject designs. In a second step, we also detailed the control group design, distinguishing active, passive, or no control group. We considered it an active control group when patients participated in usual care or unspecific activities. A passive control group referred to a waiting list or a no-treatment phase.

The statistical analysis was the third criterion. As proposed by Cicerone et al,⁷⁵ comparisons of between-group treatment conditions were considered as a higher level of methodological quality compared to within-group comparisons. We also identified whether or not the authors applied an intention-to-treat analysis. Finally, we analyzed whether the effect size and measures of variability such as confidence intervals were reported.

## Charting the data

In accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses Extension for Scoping Reviews guidelines,⁷⁶ a flow diagram was used in order to illustrate study selection (figure 1). The level of evidence for the efficacy of cognitive rehabilitation was also charted (figure 2). Figure 2 details the number of studies that met each precited methodological

criterion and associated subcriteria. For each study, the key characteristics of participants with TBI, cognitive rehabilitation, experimental design, intervention, neuropsychological outcome measures, and significant main results were collected and are summarized in table 1.

## Results

Between January 2015 and July 2021, 458 studies were published in the Pubmed (via Medline) and PsycINFO databases. We found 31 duplicates across the 2 databases and removed them (figure 1). Four hundred twenty-seven records were reviewed by title and abstract and 330 were excluded based on the inclusion and exclusion criteria. Ninety-seven articles were assessed by full-text review. In the end, 46 studies were included in the scoping review.

## Cognitive domains targeted by cognitive rehabilitation

The results showed a large scope of 7 cognitive functions targeted by interventions: executive functions (n=14, 30%), attention (n=14, 30%), memory (n=7, 15%), communication (n=4, 9%), social cognition (n=1, 2%), topographic orientation (n=1, 2%), and verbal auditory perception (n=1, 2%). Global training was proposed in 12 out of the 46 studies (26%).

## Characteristics of cognitive rehabilitation

### Type of cognitive interventions

In this review, integrative cognitive interventions concerned 48% of studies (n=22), cognitive training was reported in 37% of studies (n=17), and external aids training was described in 11% (n=5). Two studies did not detail the type of intervention (4%).⁶²,⁷⁴ The effects of combined interventions were examined in 4 studies,⁴⁶,⁴⁷,⁵²,⁵⁹ in which cognitive rehabilitation was associated with pharmacotherapy,⁴⁶ repetitive transcranial magnetic stimulation,⁵² or transcranial direct current stimulation (tDCS).⁴⁷,⁵⁹

### Methodological parameters of cognitive rehabilitation

Among the 46 reviewed studies, we showed that individual sessions were used in 83% of the studies (n=38), whereas group sessions were only used in 11% (n=5). Six percent of the studies combined individual and group sessions (n=3).

Furthermore, the length of interventions was heterogeneous, ranging from 5 days⁴⁷ to 15 months.⁶⁴ Fifty-four percent of studies proposed an intervention that lasted between 1 and 3 months (n=25). Shorter interventions lasting 1 week to 1 month were found in 24% of studies (n=11). Finally, cognitive rehabilitation interventions including a duration of <1 week or >3 months were found in 1 (2%) and 8 studies (18%), respectively. In 1 study, this methodological feature was not detailed (2%).⁴³

Concerning the intensity of interventions, 26% of the reviewed studies proposed 2 sessions per week (n=12) and 44% proposed 3 or more sessions per week (n=20). Conversely, 11% included only 1 session per week (n=5). In 1 study, the intensity was variable and progressively decreased among each phase of cognitive rehabilitation.⁶¹ Finally, 17% did not describe this methodological point (n=8).
<figure><img src="image_4.png" /><figcaption>**Fig 1** Flow diagram for the scoping review process with Preferred Reporting Items for Systematic Reviews and Meta-Analyses Extension for Scoping Reviews guidelines.</figcaption></figure>

Our results indicated that 9 out of the 46 studies did not detail both the length and intensity of the interventions (20%). Among studies that detailed length and intensity, the most common design combined 3 or more sessions per week over 1 to 3 months and was found, in this scoping review, in 10 studies.

## Behavioral examination and neuroimaging as outcome measures

The effects of cognitive rehabilitation were mostly measured with standardized neuropsychological tests in 41 out of the 46 studies (89%). Ecological neuropsychological examination was used in 35% of studies (n=16). Fifty percent included a self-report questionnaire (n=23), whereby cognitive complaint was assessed in 16 studies (70%) and quality of life was measured in 7 studies (30%). Finally, reporting by relatives was used in 35% of studies (n=16).

Thirty-seven percent of studies used one of these 4 types of measures (n=17), 28% of studies used 2 types of measures (n=13), and 24% used 3 types of measures (n=11). In contrast, 11% of studies proposed an exhaustive evaluation with these 4 types of measures (n=5).

Neuroimaging outcome measures used as brain markers of cognitive rehabilitation were reported in 20% of studies (n=9),

whereas EEG was performed in only 2 studies.⁴²,⁴³ More specifically, resting state functional magnetic resonance imaging (fMRI),⁷¹ regional cerebral blood flow,⁵² and brain activation during an fMRI cognitive task⁴⁷,⁶⁵ were analyzed in 4 studies. Structural MRI data were reported in 4 studies.³⁷,³⁸,⁴¹,⁶⁷ Only 1 paper combined diffusion tensor imaging, attention-related fMRI, and resting-state fMRI sequences.⁶⁵

## Efficacy of cognitive rehabilitation

According to Cicerone et al's criteria for evidence-based classes,⁶ 41%³¹,³²,³⁴-³⁷,⁴³,⁴⁵-⁵¹,⁵³,⁵⁸,⁶⁰,⁶⁶,⁷² of reviewed studies were classified as class I (n=19), 13%³⁰,³⁹,⁴¹,⁴⁴,⁶¹,⁶³ as class II (n=6), and 46%²⁹,³³,³⁸,⁴⁰,⁴²,⁵²,⁵⁴-⁵⁷,⁵⁹,⁶²,⁶⁴,⁶⁵,⁶⁷-⁷¹,⁷³,⁷⁴ as class III (n=21).

Ninety-three percent of studies reported significant cognitive improvement on at least 1 outcome measure, among which 19 studies described clinical improvement on the primary outcome independently of statistical change (figure 2). Within these studies, 10 were classified as class I and involved an active control group.³²,³⁴,³⁷,⁴⁰,⁴⁵,⁴⁶,⁴⁷,⁵⁰,⁵¹,⁶⁰ Then, with regard to statistical analysis, these 10 studies applied between-group comparisons to assess the efficacy of treatment, among which 7 used an intention-to-treat analysis (15% of reviewed studies).³²,³⁷,⁴⁵,⁴⁷,⁵⁰,⁵¹,⁶⁰ Medium to large effect sizes were reported in 5 out of these 7
<figure><img src="image_5.png" /><figcaption>Fig 2 Flow diagram for the level of evidence in the efficacy of cognitive rehabilitation in the reviewed studies.</figcaption></figure>

studies<sup>32,37,45,51,60</sup> and the confidence interval was reported in only 1 out of these 7 studies.<sup>51</sup>

Discussion

This scoping review was conducted starting with 2015, after the
most recent systematic review,¹⁰ in order to identify and charac-
terize studies evaluating cognitive rehabilitation after a moderate
to severe TBI, to summarize the cognitive approach used and the
domains investigated, and to analyze their efficacy.

Memory, attention, and executive functions were most often
targeted in individual sessions adopting an integrative cognitive
approach. Cognitive interventions were mainly temporally distrib-
uted with 3 or more sessions per week over 1 to 3 months. One or
2 behavioral outcome measures were mostly preferred by authors
to assess the efficacy of intervention, whereas neuroimaging out-
come measures were rarely used. The review found clinically sig-
nificant effects of cognitive rehabilitation after a moderate to
severe TBI in a very large part of reviewed studies (93%), among
which 41% described an improvement on the primary outcome
measure. The high number of positive published results could be
the sign of a publication bias according to Dwan et al's conclu-
sions in 2013.⁷⁷ Nevertheless, when methodological criteria for
the level of evidence were controlled (outcome measures, internal
validity, and statistical analysis) a significant decrease was
observed, from 93% to 15%. This significant decrease is unsatis-
factory and highlights the methodological requirements for future
studies. Challenges in TBI rehabilitation imply that cognitive
interventions must be based on a robust experimental design to
prove their efficacy and to replicate the findings on which recom-
mendations for clinical practice could be finally derived. There-
fore, this scoping review provides a complementary approach to
prior systematic reviews⁶,¹⁰⁻¹² by identifying 5 key methodologi-
cal points.

Specific experimental designs for cognitive
rehabilitation of patients with TBI

In this scoping review, 41% of reviewed studies were classified as
class I. This result highlights a continuing upward trend of ran-
domized controlled trials in cognitive rehabilitation. Indeed, Cice-
rone et al reported a percentage of class I studies ranged from
17%⁶,¹² to 20%¹¹ until 2008, which increased to 36% between
2009 and 2014. Randomized controlled trials were crucial for evi-
dence-based studies but not always relevant in rehabilitation prac-
tice, where double blind was sometimes not feasible¹¹ because the
therapist was systematically aware of the hypothesis underlying
the contents of intervention. Furthermore, experimental and con-
trol groups have to share common methodological parameters
such as delivery mode and length and intensity of rehabilitation to
allow between-group comparisons.⁷⁸ A major advance in the liter-
ature is the presence of an active control group to attest to the
specificity of the experimental intervention and to rule out the
nonspecific effects of global cognitive stimulation, such as treat-
ment effect, motivational or novelty effect, and Hawthorne
effect.⁷⁸ Statistically, the efficacy of interventions cannot be only
demonstrated using within-group analysis. Improvements must be
specific to the experimental intervention and thereby confirmed
with between-group comparisons. Effect sizes, rarely presented in
reviewed studies, are also a supplementary indicator of the effi-
cacy of cognitive interventions and should be systematically added
in the future. All of these methodological points were controlled in
1 study,⁵¹ in which the authors investigated the added effects of
psychoeducation and metacognitive strategy training in an experi-
mental group compared to an active control group with cognitive
rehabilitation including non-training-oriented tasks, with a posi-
tive effect for patients. Finally, a challenge for further group stud-
ies may be the individualization of the cognitive intervention
regarding cognitive profiles and complaints in order to compensate
for the clinical heterogeneity of TBI. Two main solutions could be
proposed for greater methodological relevance. The first is to con-
stitute toolboxes for each cognitive domain, including standard-
ized exercises with increasing levels of difficulty, like those
developed by Visch-Brink et al⁷⁹ and Van Rijn et al⁸⁰ in aphasia
therapy.⁸¹ For a single cognitive function rehabilitated, the thera-
pist will be able to choose the modalities of presentation of the
most relevant exercise to work on. The second solution is the use
of single-case experimental design. Multiple baseline design
includes a small number of patients (ie, classically at least 3 partic-
ipants), has high feasibility, and allows for an individualized
approach. The high level of evidence of single-case experimental
design lies in the repeated measurements performed during the
baseline and intervention phases in order to control for intra-indi-
vidual variance. The participant corresponds to their own control,
comparing their performance at the baseline and after the interven-
tion. Visual and statistical analysis are used to measure the effi-
cacy of intervention.⁴⁴,⁸²⁻⁸⁴

Combined cognitive interventions as an attractive
perspective

Combined interventions are interesting to potentiate significant
individual benefits of each therapy on cognitive functioning and to
promote the generalization of improvements to daily functioning.
Regarding the results of the present scoping review, combination
may be considered at 3 levels: within interventions, between deliv-
ery modes of interventions, and between interventions.

Forty-eight percent of the reviewed studies used integrative
rehabilitation combining both cognitive and metacognitive train-
ing. For example, Emmanuel et al,³² in a randomized controlled
trial of 18 patients with TBI, showed the benefits of goal manage-
ment training (GMT) associated with working memory (WM)
training (GMT+WM group) in comparison with an isolated WM
group on multistep everyday tasks and ecological executive mea-
ures, with small to large effect sizes for the combined approach.

The second level of combination was between group and indi-
vidual sessions. Even if, in this scoping review, results showed
that individual interventions remained the majority (83%), a com-
bined approach of these 2 delivery modes was proposed in 3 stud-
ies, but its specific benefits were not analyzed. ³³,⁵³,⁵⁴

The third level concerned the use of combined interventions.
Only 4 studies proposed combined rehabilitation with pharmaco-
therapy<sup>46</sup> or noninvasive brain stimulation.<sup>47,52,59</sup> The heteroge-
neous designs and the low statistical power of these studies call
for replication.

Specific effects of length and intensity of cognitive
rehabilitation

The main temporality reported by this scoping review included a
moderate duration (ie, ranging between 1 and 3 months) with a
high intensity (ie, 3 or more sessions per week). This choice seems
related to clinical relevance and feasibility in clinical research pro-
tocols. As mentioned by Cicerone et al,¹⁰ the intensity and length
of the cognitive interventions must be studied in order to deter-
mine their respective contribution to the efficacy of the rehabilita-
tion and thus have to be integrated into statistical models. None of
these 2 parameters were analyzed across all reviewed studies. Fur-
thermore, Chiaravalloti et al⁵¹ have investigated the use of
monthly booster sessions proposed over 5 months, after memory
training with 10 sessions over 5 weeks. These focused on applying

trained memory strategies in daily life. Although the authors
reported no effect of these booster sessions during follow-up, it
seems very useful to check the implementation and efficacy of
trained cognitive strategies in daily living.

In addition to length and intensity parameters, future studies
should investigate the severity of cognitive impairment at inclu-
sion, the delay from the injury, or fatigability as contributing vari-
ables in determining the dynamic of the intervention.

Selection of outcome measures as a key
experimental point

The choice of outcome measures is a key methodological point
as well as the categorization into classes I to III for evidence-
based medicine. Assessment using standardized neuropsychoso-
logical examination was the most frequently reported (89%),
followed by self-report questionnaires (50%), ecological neuro-
psychological assessment (35%), and relative report question-
naires (35%). An exhaustive neuropsychological examination
of all cognitive domains could contribute to demonstrating the
benefits of therapy on trained as well as on untrained functions.
Moreover, after a washout period, a follow-up assessment may
show maintained benefits of rehabilitation. However, it has
been well described that standardized pencil-paper neuropsy-
chological performance test could not exactly reflect those
obtained in daily contexts, especially in executive functions
assessment.⁸⁵ In this way, an ecological cognitive assessment
could be a sensitive measure to predict real-life performance.⁸⁶
Ecological tests such as the Test of Everyday Attention⁸⁷ or the
Rivermead Behavioral Memory Test⁸⁸ were frequently pro-
posed in the reviewed studies but remained in nonecological
environments and encompassed a restricted representation of
daily life tasks. Conversely, the Multiple Errands Test,⁸⁵ which
was not reported here, implies daily life activities, takes place
outside of the rehabilitation sites, and offers a more sensitive
image of executive disorders.⁸⁵ The Multiple Errands Test
should be combined with person-centered assessment to
improve the clinical relevance of the evaluation. The goal
attainment scaling,⁸⁹ derived from occupational therapy, makes
it possible to set personalized goals with the patient as well as
5 levels of predicted attainment for a sensitive evaluation of
progress.⁹⁰

In the scoping review, 2 authors developed ecological experi-
mental tasks to assess the effect of executive rehabilitation.
Emmanuel et al³² proposed multistep daily activities such as
sending a text message or buying an airplane ticket. The number
of correct steps was counted and compared among parallel scripts
before and after cognitive rehabilitation. After sessions of goal
management training, Gracey et al³⁴ defined with each participant
several daily life intentions, such as making sure their mobile
phone is with them, charged, and switched on. The daily propor-
tion of intentions achieved by patients was studied.

Finally, several studies used cognitive complaint and quality of
life questionnaires to investigate views of patients and their family
in addition to the standardized neuropsychological examination.
After cognitive rehabilitation, these reports provided an update on
the cognitive complaint and metacognitive abilities.

Exhaustiveness and specificity of assessment constitutes a
methodological key point contributing to the level of evidence of
interventions. Complete outcome measures (ie, standardized
examination, ecological assessment, self- and relative reports) were reported in only 5 studies.<sup>32,44,51,53,72</sup>

## Multiple contributions of neuroimaging in cognitive interventions

Magnetic resonance imaging was used in 20% of reviewed studies. The use of neuroimaging tools has remained scarce in recent years, which is in agreement with Galetto and Sacco,<sup>91</sup> who reported only 11 studies between 1985 and 2016 that used neuro-imaging techniques to attest to neuroplastic changes after cognitive rehabilitation in TBI. For instance, Chiaravalloti et al<sup>50</sup> reported BOLD signal changes during word learning and recognition tasks, with patterns of increased and decreased cerebral activation in the frontal and parietal lobes after 10 sessions of memory rehabilitation. Some authors have suggested a disengagement of the executive control network and an activation of the default mode network after cognitive rehabilitation to explain cognitive improvement, suggesting that memory tasks became less cognitively demanding after cognitive rehabilitation. Nevertheless, no details were given about cognitive scores on task-related functional activation.

Brain imaging constituted a promising method, but further research is needed to identify potential contributions. Structural and functional MRI continue to contribute to a better understanding of TBI physiopathology. These techniques illustrate the brain reorganization and the dynamics of plasticity mechanisms that could be associated with short- and long-term cognitive changes.

Brain imaging may also participate in the identification of potential modulators of recovery trajectories after TBI<sup>92</sup> such as brain reserve, including measures of specific patterns of gray matter volume, cortical thickness, synaptic integrity, or white matter microstructural properties. Neuroimaging could make multiple contributions, but at this time its use as a measure of the efficacy of an intervention should be done in combination with cognitive measures.

## Study limitations

A few main limitations were identified in the scoping review. The first concerned the search strategy, which focused on only 2 databases and did not include the gray literature. As reported, the effect of publication bias could contribute to an inaccurate picture of the literature on cognitive rehabilitation. Second, only 1 reviewer performed data extraction and analysis. Though we made efforts to define criteria precisely to assess the methodological quality of the reviewed studies, there may be subjective interpretation involved in this process.

## Conclusions

This scoping review highlights the persistent and growing interest in cognitive rehabilitation with major methodological improvements in the design of studies for moderate to severe TBI since 2015. This led to a higher number of studies that show an improvement in the primary outcome measures after cognitive rehabilitation. Our findings make it possible to identify 3 methodological criteria and subcriteria for determining the level of evidence of cognitive interventions and could be used in future studies. Our approach is complementary to the prior systematic

reviews<sup>6,10-12</sup> that were mainly focused on the content of interventions. Methodological efforts must be continued, and combined interventions studies must be proposed. Individualized cognitive rehabilitation also remains a challenge. Outcome measures must be well selected, including neuropsychological tests in ecological and nonecological environments, patient and relative reports. Rehabilitation of social cognition and emotion regulation should be better investigated. The results of this scoping review now need to be confirmed by systematic reviews and meta-analyses.

## Keywords

Brain injuries; Cognitive Remediation; Rehabilitation; Review

## Corresponding author

Adeline Julien, MSc, Département de neurologie, Unité de neuro-psychologie clinique, CHU de Toulouse, Place du Dr Baylac, 31059 Toulouse cedex, France. E-mail address: julien.ade@chutoulouse.fr.

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