ORIGINAL RESEARCH published: 19 June 2019 doi: 10.3389/fnbeh.2019.00135 Traumatic Brain Injury Modifies the Relationship Between Physical Activity and Global and Cognitive Health: Results From the Barcelona Brain Health Initiative Timothy P. Morris 1,2,3,4 *, Jose-Maria Tormos Muñoz 1,2,3 , Gabriele Cattaneo 1,5,6 , Javier Solana-Sánchez 1,2,3 , David Bartrés-Faz 1,5,6 and Alvaro Pascual-Leone 1,4 1 Institut Guttmann, Institut Universitari de Neurorehabilitació Adscrit a la UAB, Badalona, Spain, 2 Universitat Autònoma de Barcelona, Bellaterra, Spain, 3 Fundació Institut d’Investigació en Ciències de la Salut Germans Trias i Pujol, Barcelona, Spain, 4 Berenson-Allen Center for Noninvasive Brain Stimulation, Division of Cognitive Neurology, Department of Neurology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, United States, 5 Departament de Medicina, Facultat de Medicina i Ciències de la Salut, Universitat de Barcelona, Barcelona, Spain, 6 Institut d’Investigacions Biomediques August Pi i Sunyer (IDIBAPS), Barcelona, Spain Physical activity has many health benefits for individuals with and without history of brain injury. Here, we evaluated in a large cohort study the impact of physical activity on global and cognitive health as measured by the PROMIS global health and NeuroQoL cognitive function questionnaires. A nested case control study assessed the influence of a history of traumatic brain injury (TBI) on the effects of physical activity since underlying pathophysiology and barriers to physical activity in individuals with TBI may mean the Edited by: Frederico C. Pereira, effects of physical activity on perceived health outcomes differ compared to the general University of Coimbra, Portugal population. Those with a history of TBI (n = 81) had significantly lower Global health Reviewed by: (β = −1.66, p = 0.010) and NeuroQoL cognitive function (β = −2.65, p = 0.006) Ana Cristina De Bem Alves, Federal University of Santa Catarina, compared to healthy adults (n = 405). A similar proportion of individuals in both groups 2 Brazil reported being active compared to being insufficiently active (X(1) = 0.519 p = 0.471). Matthew J. Robson, Furthermore, the effect of physical activity on global health (β = 0.061, p = 0.076) and University of Cincinnati, United States particularly for NeuroQoL (β = 0.159, p = 0.002) was greater in those with a history of *Correspondence: Timothy P. Morris TBI. Individuals with a history of TBI can adhere to a physically active lifestyle, and if tpmorris@bidmc.harvard.edu so, that is associated with higher global and cognitive health perceptions. Adhering to a physically active lifestyle is non-trivial, particularly for individuals with TBI, and therefore Received: 15 February 2019 Accepted: 05 June 2019 adapted strategies to increase participation in physical activity is critical for the promotion Published: 19 June 2019 of public health. Citation: Keywords: physical activity, cognition, global health, traumatic brain injury, health-related quality of life Morris TP, Tormos Muñoz J-M, Cattaneo G, Solana-Sánchez J, Bartrés-Faz D and Pascual-Leone A (2019) Traumatic Brain Injury Modifies the Relationship Between Physical INTRODUCTION Activity and Global and Cognitive Health: Results From the Barcelona Physical activity is associated with a 20%–30% lower risk in all-cause mortality and incidence Brain Health Initiative. of multiple chronic conditions (James et al., 2016). Numerous governing bodies including Front. Behav. Neurosci. 13:135. the World Health Organization, American Heart Association and the American College of doi: 10.3389/fnbeh.2019.00135 Sports Medicine have focused much attention on the beneficial effects of a physically active lifestyle Frontiers in Behavioral Neuroscience | www.frontiersin.org 1 June 2019 | Volume 13 | Article 135 Morris et al. Physical Activity and Health (Warburton et al., 2006; Haskell et al., 2007; WHO, 2019a). Health Initiative1 , starting in 2017. Adults aged 40–65 were The effects span multiple bodily systems from cardiovascular invited to participate in an online questionnaire-based survey benefits (James et al., 2016) to mental health (Blumenthal et al., via television and local advertisements. The study protocol is 1999; Babyak et al., 2000) and cognitive function (Colcombe described in Cattaneo et al. (2018). All methods described and Kramer, 2003; Gomes-Osman et al., 2018; Northey et al., were approved by the education and ethics committee of 2018). The effects of physical activity on cognitive function has Institut Guttmann. This manuscript was prepared under received particular attention in recent decades across distinct the strengthening the reporting of observational studies in age groups, including adolescents (Donnelly et al., 2016), older epidemiology (STROBE) guidelines. adults (Colcombe and Kramer, 2003) and patients with dementia At the time of analysis (June 2018), a total of 4,624 individuals (Gomes-Osman et al., 2018). Physical activity represents a had enrolled. Of those, 81 individuals (1.8%) answered positively modifiable lifestyle factor capable of improving global and to the question: Have you ever had a TBI with loss of cognitive health across the lifespan. However, engaging in a consciousness? A control group (N = 405, 49% female) was physically active lifestyle is non-trivial. Globally, one in four randomly selected from the total cohort using Microsoft Excel’s adults are classified as insufficiently active (WHO, 2019b), ‘‘rand’’ function. The total cohort was organized by this random which is estimated to contribute to 9% of all premature number sequence and then filtered per the age and gender deaths worldwide (or 5.3 million; Lee et al., 2012). Physical criteria. Whereby five adults free from any neurological or inactivity is exacerbated in those with a disability, with almost psychological disorders were selected for every participant with half of US adults with a disability being physically inactive a history of TBI at random in blocks of 5 years with an even male and having a greater likelihood of having a chronic disease to female ratio. (Carroll et al., 2014). Individuals who have acquired brain injuries can become Outcomes and Covariates prone to a sedentary lifestyle which places them at risk of Our main outcome variables were perceived global health and secondary health complications (Shavelle et al., 2001). A number perceived cognitive function. To measure these constructs, of studies have reported that individuals with a history of the PROMIS global health questionnaire (Cella et al., 2010) traumatic brain injury (TBI) are insufficiently active enough to and the NeuroQoL cognitive function questionnaire (Gershon receive a health benefit (Reavenall and Blake, 2010; Hamilton et al., 2012) were used. PROMIS global health is a 10-item et al., 2015), according to current guidelines (Larry Durstine 5-point Likert scale (1-poor, 5-excellent) that probes respondents et al., 2012). The long-term health consequences of TBI include physical, mental and social health. Higher scores mean more cognitive, sensorimotor, behavioral and social problems that can of the construct is being measured (i.e., higher global health). negatively affect quality of life (Stocchetti and Zanier, 2016), NeuroQoL cognitive function is 5-point Likert scale (1-very and in the US alone, an estimated 3.2 million individuals live often, 5-never) with 12 items that probes respondents thinking, with residual effects of TBI (Benedictus et al., 2010). Cognitive attention, planning, new task learning and comprehension. dysfunction following TBI can last for decades post-injury Higher scores mean more of the construct is being measured (Draper and Ponsford, 2008) and physical exercise is a potential (i.e., better perceived cognitive function). therapeutic intervention for those living with residual effects Our main predictor variable was physical activity levels. of an injury (Hoffman et al., 2010; Wise et al., 2012; Chin We chose to implement the Godin-Shepard leisure time et al., 2015). Whilst the feasibility of dedicated and professional- physical activity questionnaire (Godin and Shephard, 1985) to led, short-to-mid-term (3 months) aerobic exercise programs in measure this. The GSLTPAQ probes the number of times spent community-dwelling individuals with moderate-to-severe TBI performing moderate (not exhausting) or strenuous (heart beats has been demonstrated (Devine et al., 2016), the association rapidly) physical activity of at least 15-min during a typical between a physically active lifestyle and global and cognitive 7-day period (Godin, 2011). The frequency score is multiplied brain health in this population has not been assessed. Distinct by a corresponding metabolic equivalent for task (MET) value barriers to performing physical activity (Rimmer et al., 2004) (moderate = ∗ 5; strenuous = ∗ 9) and summed to obtain an and underlying pathophysiology (Werner and Engelhard, 2007) arbitrary leisure score index (LSI). Cut-off points can be created may mean that this relationship differs in individuals with a using the LSI, the rationale for which originate from the history of TBI. World Organization (WHO, 2018) and American College of We performed a nested case-control study to assess the impact Sports Medicine (Ferguson, 2014) guidelines for weekly physical of a history of TBI on the associations between physical activity activity associated with significant health benefits (combination and perceived global and cognitive health. We hypothesized of moderate and strenuous activity 3–5 times per week). An that physical activity would be predictive of higher global and LSI of ≥24 is active where as those ≤23 are insufficiently cognitive health in both those with and without a history of TBI. active. Consequently, those culminating in a score of ≥24 using questions that pertain to moderate and strenuous physical MATERIALS AND METHODS activity and LSI calculations based on both frequency and energy expenditure will likely meet the physical activity guidelines. The Study Design utility and accuracy of these cut-off scores have been validated A cohort of community-dwelling adults, mainly in the Catalonia region of Spain, was established as part of the Barcelona Brain 1 www.bbhi.cat Frontiers in Behavioral Neuroscience | www.frontiersin.org 2 June 2019 | Volume 13 | Article 135 Morris et al. Physical Activity and Health in healthy adults (Amireault and Godin, 2015). Raw scores TABLE 1 | Participant characteristics and questionnaire scores between groups. above 7 for each question were excluded (N = 13) as they Healthy adults History of TBI were considered to be derived through misinterpretation of the Age (years) 51.8 (7.2) 51.7 (7.1) question. Those without responses were set to missing (N = 12). BMI (kg/m2 ) 24.2 (3.5) 24.4 (4.0) Co-variates included gender and age, which was asked in PROMIS Global Health 34.9 (4.6) 32.2 (6.2)∗ years and three categories were created; 40–49, 50–59 and 60 and PROMIS NeuroQoL 52.3 (6.5) 47.5 (11.0)∗ above. BMI was calculated as body weight (in kilograms) divided DASS21 13.4 (11.3) 20.4 (17.5)∗ by height (in meters squared). Self-perceived negative affect in GSLTPAQ 19.5 (19.2) 18.8 (18.3) depression, anxiety and stress was also assessed using the 21-item ∗ Significantat p < 0.05. GSLTPAQ, Godin-Shepard leisure time physical activity sub-scale version of the Depression Anxiety Stress Scale (Brown questionnaire. et al., 1997). This is a 4-point Likert scale (1-never, 4-always) where higher scores represent higher negative affective state. This was chosen as a potential confounder as perceived negative effect can affect how one reports cognitive and global health (Bartrés- Faz et al., 2018). Statistical Analysis We tested age, gender and negative affective status as potential confounding variables in our analysis. Variables which predicted the outcome measure with a p ≤ 0.05 were defined as confounders and added to the final model. The proportion of individuals who reported being insufficiently active compared to active was tested using Pearson’s chi squared test of proportions, as was gender. A Kruskal-Wallis test was used to assess differences in BMI between groups. Generalized linear models with a Gaussian family function and identity link function were FIGURE 1 | Hollow pie charts show the proportion of individuals who report used to assess the independent associations between physical being active (yellow bars) compared to insufficiently active (orange bars) activity levels and diagnosis history (history of TBI or not) based on the Godin-Shepard leisure time physical activity questionnaire on perceived cognitive function and perceived global health, (GSLTPAQ). The Godin questionnaire classifies people as active or controlling for all other significant variables in the model. To insufficiently active based on the number of times per week spent performing assess whether the associations between physical activity and either moderate or strenuous physical activity of at least 15 min. The inner bars represent the group with a history of traumatic brain injury (TBI) and the perceived cognitive and global health differed between those outer bars represent those free from any neurological or neuropsychiatric with and without a history of TBI, an interaction term between disease. A numerically higher proportion of individuals in both groups report physical activity and diagnosis history was added to the model. being insufficiently active compared to those reporting being active. Post estimation tests were performed using marginal effects and the estimated slopes were plotted. All statistical analyses were of global health (β = −1.66, SE = 0.644, p = 0.010, 95% performed in Stata version 15 (StataCorp LLC, College Station, CI’s = −2.927, −0.403) with those with a history of TBI TX, USA). reporting lower perceived global health (32.2 ± 0.70) than those without (34.9 ± 0.22). Physical activity level significantly RESULTS predicted Promis global health (β = 0.049, SE = 0.011, p ≤ 0.001, 95% CI’s = 0.027, 0.071). A non-significant interaction between Table 1 describes all participant characteristics and questionnaire diagnosis and physical activity level was shown (β = 0.061, scores for each group. There was no significant difference SE = 0.034, p = 0.076, 95% CI’s = −0.006, 0.128). Post estimation between the age of the participants in each group (t (116) = −0.3, tests showed that the relationship between physical activity and p ≥ 0.740) and the proportion of male and female participants 2 = 0.004 p = 0.951)]. global health was marginally greater in the group with a history was similar across groups [49% female (X(1) of TBI (β = 0.103, SE = 0.032, p = 0.001, 95% CI’s = 0.040, 0.166), BMI was not significantly different between each group 2 = 0.042 p = 0.838). than in the healthy adults (β = 0.042, SE = 0.011, p ≤ 0.001, 95% (X(1) CI’s = 0.019, 0.065; Figure 3A). Physical Activity Level Using the LSI cut-off scores to classify participants into active NeuroQoL Cognitive Function and insufficiently active, a similar proportion of those with and The distribution of NeuroQoL cognitive function scores in 2 = 0.519 without and history of TBI were classified as active (X(1) both groups is shown in Figure 2B. Diagnosis was a p = 0.471), compared to insufficiently active (Figure 1). significant predictor of NeuroQoL cognitive function (β = −2.65, SE = 0.974, p = 0.006, 95% CI’s = −4.561, −0.743), with PROMIS Global Health those with a history of TBI reporting lower perceived cognitive The distribution of Promis global health scores in both groups function health (47.45 ± 1.20) than those without (52.26 ± 3.29). is shown in Figure 2A. Diagnosis was a significant predictor Physical activity level was predictive of NeuroQoL cognitive Frontiers in Behavioral Neuroscience | www.frontiersin.org 3 June 2019 | Volume 13 | Article 135 Morris et al. Physical Activity and Health FIGURE 2 | Histogram plots show the distribution of scores on the global health scale (A) and the NeuroQoL cognitive function scale (B) for both participants in the healthy group (orange filled bars) and the group with a history of TBI (black outlined bars). FIGURE 3 | Scatter plots of the relationship between physical activity levels and the predicted Global health and NeuroQoL cognitive function scores as a result of the generalized linear models, by group. (A) A trending interaction (p = 0.076) was observed between groups whereby the group with a history of TBI had a greater effect of physical activity level on global health (navy line). In (B) a significant interaction between groups is observed (p = 0.002) whereby the group with a history of TBI shows a significant effect of physical activity on NeuroQoL cognitive function, which is not significant for the group without a history of TBI (red line). function (β = 0.037, SE = 0.016, p ≤ 0.023, 95% CI’s = 0.005, found that individuals with a history of TBI were as likely to be 0.070). A significant interaction between diagnosis and physical physically active as those without a history of TBI and physical activity level was shown (β = 0.159, SE = 0.051, p = 0.002, activity levels were even stronger predictors of both global and 95% CI’s = 0.058, 0.260) whereby post estimation tests showed cognitive function health perceptions than in individuals without that the relationship between physical activity and NeuroQoL a history of TBI. cognitive function was significant in the group with a history of Self-reported levels of physical activity have been associated TBI (β = 0.179, SE = 0.049, p ≤ 0.001, 95% CI’s = 0.083, 0.274), with numerous protective health benefits such as reduced risk of but not in the healthy adults (β = 0.019, SE = 0.017, p = 0.260, cognitive impairment (Laurin et al., 2001) and cognitive decline 95% CI’s = −0.014, 0.054; Figure 3B). (Sofi et al., 2011), mortality due to cardiovascular disease (Nocon et al., 2008) and reduced incident rates of dementia (Larson DISCUSSION et al., 2006). Self-report physical activity has also been associated with better health-related quality of life (HRQOL; Brown et al., In this study, we aimed to assess the impact of a history of 2003). These findings from the 2001 behavioral risk factor TBI on the relationship between physical activity levels and surveillance system survey found that adhering to recommended global and cognitive brain health. Not surprisingly, we found levels of physical activity was significantly associated with less that healthy adults reported higher global and cognitive brain days of poor perceived mental and physical health. Our results health compared to those with a history of TBI. However, we also corroborate these findings in so much as higher physical activity Frontiers in Behavioral Neuroscience | www.frontiersin.org 4 June 2019 | Volume 13 | Article 135 Morris et al. Physical Activity and Health levels are related to higher perceptions of global (mental, with a disability or a TBI have distinct barriers to engaging in physical, social and pain) health. Thereupon, physical activity physical activity (Rimmer et al., 2004; Reavenall and Blake, 2010; appears not only associated with improved health outcomes but Pinto et al., 2018), including but not limited to having health with higher perceptions of health also. concerns and lack of counselling by a physician (Pinto et al., Numerous randomized-control trials have shown positive 2018). Therefore, strategies to increase adherence to a physically associations between physical activity and physical exercise and active lifestyle, such as the WHO’s Global Strategy on Diet and cognitive function (Colcombe and Kramer, 2003; Gomes-Osman Physical Activity (Bauman and Craig, 2005), are not only critical et al., 2018). Additionally, a number of these studies have also for both the general population and community-dwelling adults shown improvements in the structure and function of cortical with a history of TBI but may need to be adapted to those living networks associated with cognitive functioning (Erickson et al., with a history of TBI. Promising results from a feasibility study 2011; Voss et al., 2013; Weng et al., 2017). Whilst dose-response of aerobic exercise programs in community-dwelling individuals studies are limited (Vidoni et al., 2015; Chen et al., 2018), a linear with a history of moderate-to-severe TBI showed that greater relationship between physical activity and health status has been adherence to exercise was achieved when free access to local reported, such that increases in physical activity leads to greater gymnasiums was provided (Devine et al., 2016). Our results health benefits, especially in previously sedentary individuals suggest that strategies like these that will increase adherence to a (Warburton et al., 2006). Our results, however, failed to show physically active lifestyle, will likely lead to improved perceptions any association between physical activity levels and perceptions of global and cognitive health. of cognitive functioning in middle to older aged adults free Our study has certain limitations that may limit the from any neurological or neuropsychiatric disease. This may interpretation of the results. Self-reported health outcomes, be explained by the difference in the characteristics of the specifically TBI can be problematic and whilst sports concussion included participants in our analysis whereby those with a history research has improved the self-reporting of concussion through of TBI had significantly lower NeuroQoL scores compared to better descriptions of concussion definitions (Robbins et al., those without a history of TBI. This could have been further 2014), this type of description is less well defined for the general exacerbated by a ceiling effect in the NeuroQoL scale for the public. Though the accuracy of self-reported measures of certain healthy adult population. This scale was developed to assess health outcomes (including stroke) have been documented cognitive complaints in those with neurological afflictions and (Okura et al., 2004), self-reported measures are often the best so may fail to capture a large enough variance in cognitive tool available, especially for large cohort studies. Given this health perceptions amongst healthy adults (Gershon et al., 2012). constraint, we did not assess the severity of an individual’s TBI Additionally, perceptions of cognitive function may not correlate nor the time since injury in our cohort of TBI. Whilst this should well with objective measures of cognitive functioning, which is not affect the exposure/outcome relationship, it means that we the case in a number of clinical populations (Schiehser et al., cannot be certain whether different injury severities are more or 2011; Hutchinson et al., 2012). Consequently, whilst it may be the less associated with the results found. This might be of interest case that those with lower perceptions of cognitive health receive to future studies. Additionally, if co-morbid medical conditions a greater benefit of adhering to a physically active lifestyle, studies were reported in the history of TBI group, they were not excluded with objective measures of cognitive functioning may further from the analysis. Nevertheless, the number of participants in help delineate this relationship. this group who had multiple conditions was small (headache Some concepts of HRQOL in TBI overlap with those of the (Lee et al., 2012), chronic pain (Babyak et al., 2000), anxiety general population yet research suggests that HRQOL following (Gomes-Osman et al., 2018), depression (Blumenthal et al., TBI may be more complex (Carlozzi et al., 2011). We saw 1999), memory loss (James et al., 2016), heart attack (Warburton that individuals with a history of TBI had significantly lower et al., 2006), sleep apnea (Haskell et al., 2007), arthritis (James self-reported global and cognitive brain health compared to et al., 2016) and so are unlikely to have significantly affected neurologically healthy adults. Whilst we cannot be certain that the results. this lower perception of global and cognitive brain health is derived from the injury, previous reports have shown CONCLUSION many individuals with a history of TBI live with residual negative effects of the injury (Benedictus et al., 2010). Cognitive Adhering to a physically active lifestyle is associated with dysfunction is prevalent post-injury and deficits can be seen higher global and cognitive health perceptions, especially in at 6 months (Dikmen et al., 2009) and for as long as individuals with a history of TBI. Notwithstanding, a majority 10 years after injury (Draper and Ponsford, 2008). Long-term of individuals are insufficiently active and therefore it is critical lifestyle interventions aimed at reducing these deficits are to develop strategies to increase adherence to and participation therefore of great importance to those living with residual in a physically active lifestyle in both those with and without a effects of TBI. history of TBI. We found that a similar proportion of those adults with a history of TBI reported being active as those without a history DATA AVAILABILITY of TBI. However, a numerical majority of participants (both in the history of TBI and healthy group) were classified as The raw data supporting the conclusions of this manuscript will insufficiently active. Previous research has suggested that those be made available by the authors, without undue reservation, to Frontiers in Behavioral Neuroscience | www.frontiersin.org 5 June 2019 | Volume 13 | Article 135 Morris et al. Physical Activity and Health any qualified researcher. The datasets generated for this study are R01HD069776, R01NS073601, R21 NS082870, R21 MH099196, available on request to the corresponding author. R21 NS085491, R21 HD07616), the Football Players Health Study at Harvard University, and Harvard Catalyst | The ETHICS STATEMENT Harvard Clinical and Translational Science Center (NCRR and the NCATS NIH, UL1 RR025758). The content is solely the This study was carried out in accordance with the responsibility of the authors and does not necessarily represent recommendations of the ethics and education committee the official views of Harvard Catalyst, Harvard University and of Institut Guttmann with written informed consent from its affiliated academic healthcare centers, the National Institutes all subjects. All subjects gave written informed consent in of Health, the Sidney R. Baer Jr. Foundation. The BBHI receives accordance with the Declaration of Helsinki. The protocol was funding from ‘‘Obra Social La Caixa’’ (grant agreement n◦ approved by the ‘‘Institut Guttmann.’’ LCF/PR/PR16/11110004) and the Abertis foundation, as well as internal funding from the Institut Guttmann (Institut Guttmann AUTHOR CONTRIBUTIONS and Fundació Abertis). AP-L, DB-F and J-MTM performed the initial conception of the ACKNOWLEDGMENTS project. GC and JS-S collected the data. TM analyzed the data. TM drafted the manuscript and all authors critically revised it for A special thanks is extended to all study participants intellectual content. and other partners of the BBHI (Ad-Salutem Institute, Sodexo, I.C.A. Informática y Comunicaciones Avanzadas, FUNDING Neuroelectrics, Corporació Catalana de Mitjans Audiovisuals, Club Metropolitan, Casa Ametller, and Agéncia de Qualitat AP-L was partly supported by the Sidney R. Baer Jr. Foundation, i Avaluació Sanitáries de Catalunya-AQuAS) for their the National Institutes of Health (NIH; R01MH100186, invaluable collaboration. REFERENCES activity—United States, 2009–2012. Morb. Mortal. Wkly. Rep. 63, 407–413. Amireault, S., and Godin, G. (2015). The Godin-Shephard leisure-time physical Cattaneo, G., Bartrés-Faz, D., Morris, T. P., Sánchez, J. S., Macià, D., Tarrero, C., activity questionnaire: validity evidence supporting its use for classifying et al. (2018). 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The remaining authors declare that the research was conducted in the absence of (2004). Agreement between self-report questionnaires and medical record data any commercial or financial relationships that could be construed as a potential was substantial for diabetes, hypertension, myocardial infarction and stroke but conflict of interest. not for heart failure. J. Clin. Epidemiol. 57, 1096–1103. doi: 10.1016/j.jclinepi. 2004.04.005 Copyright © 2019 Morris, Tormos Muñoz, Cattaneo, Solana-Sánchez, Bartrés-Faz Pinto, S. M., Newman, M. A., and Hirsch, M. A. (2018). Perceived barriers to and Pascual-Leone. This is an open-access article distributed under the terms exercise in adults with traumatic brain injury vary by age. J. Funct. Morphol. of the Creative Commons Attribution License (CC BY). The use, distribution or Kinesiol. 3:47. doi: 10.3390/jfmk3030047 reproduction in other forums is permitted, provided the original author(s) and the Reavenall, S., and Blake, H. (2010). Determinants of physical activity participation copyright owner(s) are credited and that the original publication in this journal following traumatic brain injury. Int. J. Ther. Rehabil. 17, 360–369. is cited, in accordance with accepted academic practice. No use, distribution or doi: 10.12968/ijtr.2010.17.7.48893 reproduction is permitted which does not comply with these terms. Frontiers in Behavioral Neuroscience | www.frontiersin.org 7 June 2019 | Volume 13 | Article 135