Acute and protracted disruptions to inhibitory control following sports-related concussion

Extant evidence demonstrates disruptions to inhibitory control from as little as six months to as long as several years following sports-related concussion. However, the sensitivity of tasks requiring inhibitory control for detecting disruptions to cognition during the acute, subacute, and protracted phases of recovery remains in question. Accordingly, the purpose of this study was to examine concussion-related disruptions to inhibitory control across recovery. Athletes with sports-related concussion (n = 55; 22 female) completed an inhibitory control task within 72 h of injury, after returning to play, and within one month following return to play. Matched control athletes (n = 55; 22 female) were tested at similar intervals. Behavioral indices of performance were analyzed using univariate multi-level modeling. Findings indicated that the concussion group exhibited decrements to inhibitory control immediately after injury and up to one month following return to play, with no such observable differences at the return to play period. In addition to being sensitive to detecting chronic cognitive deficits resulting from sports-related concussion, these findings suggest that inhibitory control measures have the requisite sensitivity to identify the immediate and protracted signs of neurocognitive dysfunction following sports-related concussion. Accordingly, integrating assessments of inhibitory control into baseline, post-injury, and post-season measurement of cognitive function may prove useful for tracking the acute and persistent effects of sports-related concussion across an athlete's career. Athletes exhibiting impaired inhibitory control across the phases of recovery may be at greater risk of reinjury, thereby suggesting that integrating inhibitory control assessments into existing clinical measures may be of interest for informing concussion management and return-to-play decisions.

[1]  P. London.  Injury , 1969, Definitions.

[2]  C. Hillman,et al.  The persistent influence of pediatric concussion on attention and cognitive control during flanker performance , 2015, Biological Psychology.

[3]  Steven P Broglio,et al.  Cognitive Decline and Aging: The Role of Concussive and Subconcussive Impacts , 2012, Exercise and sport sciences reviews.

[4]  Tracey Covassin,et al.  Preliminary Evidence for Differential Trajectories of Recovery for Cognitive Flexibility Following Sports-Related Concussion , 2018, Neuropsychology.

[5]  S. Marshall,et al.  Postural Stability and Neuropsychological Deficits After Concussion in Collegiate Athletes. , 2001, Journal of athletic training.

[6]  R. Tallarida,et al.  The Dose—Response Relation , 1979 .

[7]  Sébastien Tremblay,et al.  Brain Function Decline in Healthy Retired Athletes who Sustained their Last Sports Concussion in Early Adulthood , 2009, NeuroImage.

[8]  Edgar Erdfelder,et al.  G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences , 2007, Behavior research methods.

[9]  Per B. Brockhoff,et al.  lmerTest Package: Tests in Linear Mixed Effects Models , 2017 .

[10]  K. Barlow.  Traumatic brain injury. , 2013, Handbook of clinical neurology.

[11]  D. Hovda,et al.  The new neurometabolic cascade of concussion. , 2014, Neurosurgery.

[12]  Regina C. Armstrong,et al.  Myelin and oligodendrocyte lineage cells in white matter pathology and plasticity after traumatic brain injury , 2016, Neuropharmacology.

[13]  N. Mohtadi,et al.  Evidence-Based Review of Sport-Related Concussion: Clinical Science , 2001, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[14]  C. Hillman,et al.  Exercise improves behavioral, neurocognitive, and scholastic performance in children with attention-deficit/hyperactivity disorder. , 2013, The Journal of pediatrics.

[15]  G. Fernández,et al.  How mild traumatic brain injury may affect declarative memory performance in the post-acute stage. , 2010, Journal of neurotrauma.

[16]  D. Stuss,et al.  Reaction time and variability 5 and 10 years after traumatic brain injury. , 1996, Brain injury.

[17]  Jason P. Mihalik,et al.  The Relationship Between Subconcussive Impacts and Concussion History on Clinical Measures of Neurologic Function in Collegiate Football Players , 2011, Annals of Biomedical Engineering.

[18]  Bruce D. McCandliss,et al.  Testing the Efficiency and Independence of Attentional Networks , 2002, Journal of Cognitive Neuroscience.

[19]  J. Heckman,et al.  A gradient of childhood self-control predicts health, wealth, and public safety , 2011, Proceedings of the National Academy of Sciences.

[20]  J. Nigg.  On inhibition/disinhibition in developmental psychopathology: views from cognitive and personality psychology and a working inhibition taxonomy. , 2000, Psychological bulletin.

[21]  T. Covassin,et al.  Depression and neurocognitive performance after concussion among male and female high school and collegiate athletes. , 2012, Archives of physical medicine and rehabilitation.

[22]  Erin D. Bigler,et al.  Neuropathology of mild traumatic brain injury: relationship to neuroimaging findings , 2012, Brain Imaging and Behavior.

[23]  M. Lovell,et al.  Sensitivity and specificity of the ImPACT Test Battery for concussion in athletes. , 2006, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[24]  J. Stroop.  Studies of interference in serial verbal reactions. , 1992 .

[25]  Christopher R. Johnson,et al.  The Relation of Mild Traumatic Brain Injury to Chronic Lapses of Attention , 2012, Research quarterly for exercise and sport.

[26]  Gerard Riedy,et al.  Postconcussional disorder and PTSD symptoms of military‐related traumatic brain injury associated with compromised neurocircuitry , 2014, Human brain mapping.

[27]  Pratik Mukherjee,et al.  Structural dissociation of attentional control and memory in adults with and without mild traumatic brain injury. , 2008, Brain : a journal of neurology.

[28]  D. Ellemberg,et al.  Prolonged Neuropsychological Impairments Following a First Concussion in Female University Soccer Athletes , 2007, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[29]  S. Lilienfeld,et al.  A meta-analytic review of the relation between antisocial behavior and neuropsychological measures of executive function. , 2000, Clinical psychology review.

[30]  C W Eriksen,et al.  Information processing in visual search: A continuous flow conception and experimental results , 1979, Perception & psychophysics.

[31]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[32]  C. Hillman,et al.  The persistent influence of concussion on attention, executive control and neuroelectric function in preadolescent children. , 2016, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[33]  J Scott Delaney,et al.  Concussions Among University Football and Soccer Players , 2002, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[34]  S. MacDonald,et al.  Intra-individual variability in behavior: links to brain structure, neurotransmission and neuronal activity , 2006, Trends in Neurosciences.

[35]  B. Ang,et al.  Chronic impairment of prospective memory after mild traumatic brain injury. , 2010, Journal of neurotrauma.

[36]  C. Hillman,et al.  The persistent influence of concussive injuries on cognitive control and neuroelectric function. , 2014, Journal of athletic training.

[37]  G. Kesteven,et al.  The Coefficient of Variation , 1946, Nature.

[38]  E. London,et al.  Inhibitory Control Deficits in Childhood and Risk for Substance Use Disorders: A Review , 2008, The American journal of drug and alcohol abuse.

[39]  K Bennell,et al.  Computerised cognitive assessment of concussed Australian Rules footballers , 2001, British journal of sports medicine.

[40]  Edgar C Merkle,et al.  Using trial-level data and multilevel modeling to investigate within-task change in event-related potentials. , 2018, Psychophysiology.

[41]  C. Hillman,et al.  Concussion does not impact intraindividual response time variability. , 2007, Neuropsychology.

[42]  M. Esiri,et al.  Axonal damage: a key predictor of outcome in human CNS diseases. , 2003, Brain : a journal of neurology.

[43]  Matthew B. Pontifex,et al.  The association between mild traumatic brain injury history and cognitive control , 2009, Neuropsychologia.

[44]  Peter A. Ornstein,et al.  Learning to Remember: Social-Communicative Exchanges and the Development of Children's Memory Skills. , 2004 .

[45]  Robert D. Catena,et al.  Spatial orientation of attention and obstacle avoidance following concussion , 2009, Experimental Brain Research.

[46]  A. Diamond.  Executive functions. , 2014, Handbook of clinical neurology.

[47]  S. E. Wall,et al.  Neuropsychological dysfunction following repeat concussions in jockeys , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[48]  J. Barth,et al.  Neuropsychology of sports-related head injury: Dementia Pugilistica to Post Concussion Syndrome. , 1999, The Clinical neuropsychologist.

[49]  D B McKeag,et al.  Relationship between concussion and neuropsychological performance in college football players. , 1999, JAMA.

[50]  D. Graham,et al.  Neuropathology of the Head Injuries. , 1998, Seminars in clinical neuropsychiatry.

[51]  Matthew B. Pontifex,et al.  The association between a history of concussion and variability in behavioral and neuroelectric indices of cognition. , 2015, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[52]  L. Osternig,et al.  Executive Dysfunction Assessed with a Task-Switching Task following Concussion , 2014, PloS one.

[53]  J. Bailes,et al.  An overview of the basic science of concussion and subconcussion: where we are and where we are going. , 2012, Neurosurgical focus.

[54]  R. Conley,et al.  Assessment of capacity to give consent to research participation: state-of-the-art and beyond. , 1998, Journal of health care law & policy.

[55]  Charles E. Brown.  Coefficient of Variation , 1998 .

[56]  L R Osternig,et al.  Attentional deficits in concussion , 2005, Brain injury.

[57]  Jared M. Bruce,et al.  Delayed-onset deficits in verbal encoding strategies among patients with mild traumatic brain injury. , 2003, Neuropsychology.

[58]  D. Katz,et al.  Update of Neuropathology and Neurological Recovery After Traumatic Brain Injury , 2005, The Journal of head trauma rehabilitation.

[59]  L. Julian,et al.  Neuropsychological Test Performance Prior To and Following Sports-Related Mild Traumatic Brain Injury , 2001, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[60]  E. Bigler.  Neuropathology of Mild Traumatic Brain Injury , 2015 .

[61]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[62]  J. Taunton,et al.  Myelin Water Fraction Is Transiently Reduced after a Single Mild Traumatic Brain Injury – A Prospective Cohort Study in Collegiate Hockey Players , 2016, PloS one.

[63]  H. Belanger,et al.  The neuropsychological impact of sports-related concussion: A meta-analysis , 2005, Journal of the International Neuropsychological Society.

[64]  L. Osternig,et al.  Tracking the recovery of visuospatial attention deficits in mild traumatic brain injury. , 2006, Brain : a journal of neurology.

[65]  N. Mohtadi,et al.  Evidence-Based Review of Sport-Related Concussion: Basic Science , 2001, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[66]  Daniël Lakens,et al.  Calculating and reporting effect sizes to facilitate cumulative science: a practical primer for t-tests and ANOVAs , 2013, Front. Psychol..

[67]  Mark T. Greenberg,et al.  The Contribution of Inhibitory Control to Preschoolers' Social-Emotional Competence. , 2009 .

[68]  M. Lezak,et al.  A Dose-Response Relation of Headers and Concussions With Cognitive Impairment in Professional Soccer Players , 2001, Journal of clinical and experimental neuropsychology.

[69]  Donald T. Stuss,et al.  Characterization of stability of performance in patients with traumatic brain injury: Variability and consistency on reaction time tests. , 1994 .

[70]  L. Osternig,et al.  Effects of concussion on attention and executive function in adolescents. , 2013, Medicine and science in sports and exercise.