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Loss of Motor Stability After Sports-Related Concussion: Opportunities for Motor Learning Strategies to Reduce Musculoskeletal Injury Risk

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Abstract

Current best practices to direct recovery after sports-related concussion (SRC) typically require asymptomatic presentation at both rest and during a graduated exercise progression, and cognitive performance resolution. However, this standard of care results in a significantly elevated risk for musculoskeletal (MSK) injury after return-to-sport (RTS). The elevated risk is likely secondary to, in part, residual neurophysiological and dual-task motor stability deficits that remain despite RTS. These deficits present as a loss of autonomous control of gait and posture and an increased need for cognition for motor stability. Thus, the incorporation of strategies that can enhance motor stability and restore autonomous control of gait and posture during SRC recovery and RTS progression may facilitate a reduction of the elevated risk of secondary MSK injury. We provide a theoretical framework for the application of motor learning principles to restore autonomous gait and postural stability after SRC via incorporation, or targeted manipulation, of external focus, enhanced expectations, autonomy support, practice schedule variability, and dual-task strategies during rehabilitation and RTS training.

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References

  1. Bryan MA, Rowhani-Rahbar A, Comstock RD, Rivara F, Seattle Sports Concussion Research Collaborative. Sports- and recreation-related concussions in US youth. Pediatrics. 2016;138:e20154635.

    Article  PubMed  Google Scholar 

  2. Reneker JC, Babl R, Flowers MM. History of concussion and risk of subsequent injury in athletes and service members: a systematic review and meta-analysis. Musculoskelet Sci Pract. 2019;42:173–85.

    Article  PubMed  Google Scholar 

  3. McPherson AL, Nagai T, Webster KE, Hewett TE. Musculoskeletal injury risk after sport-related concussion: a systematic review and meta-analysis. Am J Sports Med. 2019;47:1754–62.

    Article  PubMed  Google Scholar 

  4. Lynall RC, Mauntel TC, Pohlig RT, Kerr ZY, Dompier TP, Hall EE, et al. Lower extremity musculoskeletal injury risk after concussion recovery in high school athletes. J Athl Train. 2017;52:1028–34.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Lynall RC, Mauntel TC, Padua DA, Mihalik JP. Acute lower extremity injury rates increase after concussion in college athletes. Med Sci Sports Exerc. 2015;47:2487–92.

    Article  PubMed  Google Scholar 

  6. Fino PC, Becker LN, Fino NF, Griesemer B, Goforth M, Brolinson PG. Effects of recent concussion and injury history on instantaneous relative risk of lower extremity injury in division i collegiate athletes. Clin J Sport Med. 2019;29:218–23.

    Article  PubMed  Google Scholar 

  7. Howell DR, Lynall RC, Buckley TA, Herman DC. Neuromuscular control deficits and the risk of subsequent injury after a concussion: a scoping review. Sports Med. 2018;48:1097–115.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Parker TM, Osternig LR, van Donkelaar P, Chou L-S. Gait stability following concussion. Med Sci Sports Exerc. 2006;38:1032–40.

    Article  PubMed  Google Scholar 

  9. Zazulak B, Cholewicki J, Reeves NP. Neuromuscular control of trunk stability: clinical implications for sports injury prevention. J Am Acad Orthop Surg. 2008;16:497–505.

    Article  PubMed  Google Scholar 

  10. McCrory P, Meeuwisse W, Dvorak J, Aubry M, Bailes J, Broglio S, et al. Consensus statement on concussion in sport—the 5th international conference on concussion in sport held in Berlin, October 2016. Br J Sports Med. 2017;51:838–47.

    PubMed  Google Scholar 

  11. Howell DR, Osternig LR, Chou L-S. Single-task and dual-task tandem gait test performance after concussion. J Sci Med Sport. 2017;20:622–6.

    Article  PubMed  Google Scholar 

  12. Howell DR, Osternig L, Van Donkelaar P, Mayr U, Chou L-S. Effects of concussion on attention and executive function in adolescents. Med Sci Sports Exerc. 2013;45:1030–7.

    Article  PubMed  Google Scholar 

  13. Howell DR, Osternig LR, Chou L-S. Dual-task effect on gait balance control in adolescents with concussion. Arch Phys Med Rehabil. 2013;94:1513–20.

    Article  PubMed  Google Scholar 

  14. Howell DR, Buckley TA, Lynall RC, Meehan WP. Worsening dual-task gait costs after concussion and their association with subsequent sport-related injury. J Neurotrauma. 2018;35:1630–6.

    Article  PubMed  Google Scholar 

  15. Slobounov SM, Zhang K, Pennell D, Ray W, Johnson B, Sebastianelli W. Functional abnormalities in normally appearing athletes following mild traumatic brain injury: a functional MRI study. Exp Brain Res. 2010;202:341–54.

    Article  PubMed  Google Scholar 

  16. Kleiner M, Wong L, Dubé A, Wnuk K, Hunter SW, Graham LJ. Dual-task assessment protocols in concussion assessment: a systematic literature review. J Orthop Sports Phys Ther. 2018;48:87–103.

    Article  PubMed  Google Scholar 

  17. Buckley TA, Munkasy BA, Tapia-Lovler TG, Wikstrom EA. Altered gait termination strategies following a concussion. Gait Posture. 2013;38:549–51.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Chou L-S, Kaufman KR, Walker-Rabatin AE, Brey RH, Basford JR. Dynamic instability during obstacle crossing following traumatic brain injury. Gait Posture. 2004;20:245–54.

    Article  PubMed  Google Scholar 

  19. Fitts PM, Posner MI. Human performance. Belmont: Brooks/Cole Pub. Co.; 1967.

    Google Scholar 

  20. Bernshteĭn NA. The co-ordination and regulation of movements. Oxford; New York: Pergamon Press; 1967. http://books.google.com/books?id=F9dqAAAAMAAJ. Cited 15 Dec 2020

  21. Schaefer SY, Lang CE. Using dual tasks to test immediate transfer of training between naturalistic movements: a proof-of-principle study. J Mot Behav. 2012;44:313–27.

    Article  PubMed  Google Scholar 

  22. Howell DR, Kirkwood MW, Provance A, Iverson GL, Meehan WP. Using concurrent gait and cognitive assessments to identify impairments after concussion: a narrative review. Concussion. 2018;3:CNC54.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Kal E, Prosée R, Winters M, van der Kamp J. Does implicit motor learning lead to greater automatization of motor skills compared to explicit motor learning? A systematic review. PLoS ONE. 2018;13:e0203591.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Gagne RM, Foster H, Crowley ME. The measurement of transfer of training. Psychol Bull. 1948;45:97–130.

    Article  CAS  PubMed  Google Scholar 

  25. Abernethy B. Dual-task methodology and motor skills research: some applications and methodological constraints. J Hum Mov Stud. 1988. https://scinapse.io/papers/96422112. Cited 15 Dec 2020.

  26. Fino PC, Parrington L, Pitt W, Martini DN, Chesnutt JC, Chou L-S, et al. Detecting gait abnormalities after concussion or mild traumatic brain injury: a systematic review of single-task, dual-task, and complex gait. Gait Posture. 2018;62:157–66.

    Article  PubMed  Google Scholar 

  27. Bonnette S, Diekfuss JA, Grooms D, Myer GD, Meehan WP, Howell DR. Integrated linear and nonlinear trunk dynamics identify residual concussion deficits. Neurosci Lett. 2020;Jun;729:134975.

  28. Lee H, Sullivan SJ, Schneiders AG. The use of the dual-task paradigm in detecting gait performance deficits following a sports-related concussion: A systematic review and meta-analysis. J Sci Med Sport. 2013;16:2–7.

    Article  PubMed  Google Scholar 

  29. Howell DR, Stracciolini A, Geminiani E, Meehan WP. Dual-task gait differences in female and male adolescents following sport-related concussion. Gait Posture. 2017;54:284–9.

    Article  PubMed  Google Scholar 

  30. Parker TM, Osternig LR, Lee H-J, van Donkelaar P, Chou L-S. The effect of divided attention on gait stability following concussion. Clin Biomech. 2005;20:389–95.

    Article  Google Scholar 

  31. Catena RD, van Donkelaar P, Chou L-S. The effects of attention capacity on dynamic balance control following concussion. J NeuroEngineering Rehabil. 2011;8:8.

    Article  Google Scholar 

  32. Catena RD, van Donkelaar P, Chou L-S. Cognitive task effects on gait stability following concussion. Exp Brain Res. 2007;176:23–31.

    Article  PubMed  Google Scholar 

  33. Howell DR, Osternig LR, Chou L-S. Adolescents Demonstrate Greater Gait Balance Control Deficits After Concussion Than Young Adults. Am J Sports Med. 2015;43:625–32.

    Article  PubMed  Google Scholar 

  34. Howell DR, Osternig LR, Koester MC, Chou L-S. The effect of cognitive task complexity on gait stability in adolescents following concussion. Exp Brain Res. 2014;232:1773–82.

    Article  PubMed  Google Scholar 

  35. Springer S, Gottlieb U. Effects of dual-task and walking speed on gait variability in people with chronic ankle instability: a cross-sectional study. BMC Musculoskelet Disord. 2017;18:316.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Fino PC. A preliminary study of longitudinal differences in local dynamic stability between recently concussed and healthy athletes during single and dual-task gait. J Biomech. 2016;49:1983–8.

    Article  PubMed  Google Scholar 

  37. Sethi A, Patterson T, McGuirk T, Patten C, Richards LG, Stergiou N. Temporal structure of variability decreases in upper extremity movements post stroke. Clin Biomech (Bristol, Avon). 2013;28:134–9.

    Article  Google Scholar 

  38. Moraiti C, Stergiou N, Ristanis S, Georgoulis AD. ACL deficiency affects stride-to-stride variability as measured using nonlinear methodology. Knee Surg Sports Traumatol Arthrosc. 2007;15:1406–13.

    Article  PubMed  Google Scholar 

  39. Cavanaugh JT, Guskiewicz KM, Giuliani C, Marshall S, Mercer VS, Stergiou N. Recovery of postural control after cerebral concussion: new insights using approximate entropy. J Athl Train. 2006;41:305–13.

    PubMed  PubMed Central  Google Scholar 

  40. Cavanaugh JT. Detecting altered postural control after cerebral concussion in athletes with normal postural stability. Br J Sports Med. 2005;39:805–11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Guimarães AN, Ugrinowitsch H, Dascal JB, Porto AB, Okazaki VHA. Freezing degrees of freedom during motor learning: a systematic review. Mot Control. 2020;24(3):457–71.

    Article  Google Scholar 

  42. Wu T, Hallett M, Chan P. Motor automaticity in Parkinson’s disease. Neurobiol Dis. 2015;82:226–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Chen J, Johnston KM, Collie A, McCrory P, Ptito A. A validation of the post concussion symptom scale in the assessment of complex concussion using cognitive testing and functional MRI. J Neurol Neurosurg Psychiatry. 2007;78:1231–8.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Chiu S-L, Osternig L, Chou L-S. Concussion induces gait inter-joint coordination variability under conditions of divided attention and obstacle crossing. Gait Posture. 2013;38:717–22.

    Article  PubMed  Google Scholar 

  45. Dubose DF, Herman DC, Jones DL, Tillman SM, Clugston JR, Pass A, et al. Lower extremity stiffness changes after concussion in collegiate football players. Med Sci Sports Exerc. 2017;49:167–72.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Register-Mihalik JK, Littleton AC, Guskiewicz KM. Are divided attention tasks useful in the assessment and management of sport-related concussion? Neuropsychol Rev. 2013;23:300–13.

    Article  PubMed  Google Scholar 

  47. Pearce AJ, Tommerdahl M, King DA. Neurophysiological abnormalities in individuals with persistent post-concussion symptoms. Neuroscience. 2019;408:272–81.

    Article  CAS  PubMed  Google Scholar 

  48. O’Connell B, Kelly ÁM, Mockler D, Orešič M, Denvir K, Farrell G, et al. Use of blood biomarkers in the assessment of sports-related concussion—a systematic review in the context of their biological significance. Clin J Sport Med. 2018;28:561–71.

    Article  PubMed  Google Scholar 

  49. Bigler ED, Finuf C, Abildskov TJ, Goodrich-Hunsaker NJ, Petrie JA, Wood D-M, et al. Cortical thickness in pediatric mild traumatic brain injury including sports-related concussion. Int J Psychophysiol. 2018;132:99–104.

    Article  PubMed  Google Scholar 

  50. Kamins J, Bigler E, Covassin T, Henry L, Kemp S, Leddy JJ, et al. What is the physiological time to recovery after concussion? A systematic review. Br J Sports Med. 2017;51:935–40.

    Article  PubMed  Google Scholar 

  51. Chamard E, Lassonde M, Henry L, Tremblay J, Boulanger Y, De Beaumont L, et al. Neurometabolic and microstructural alterations following a sports-related concussion in female athletes. Brain Inj. 2013;27:1038–46.

    Article  PubMed  Google Scholar 

  52. Wilkerson GB, Grooms DR, Acocello SN. Neuromechanical considerations for postconcussion musculoskeletal injury risk management. Curr Sports Med Rep. 2017;16:419–27.

    Article  PubMed  Google Scholar 

  53. Wu Y-C, Harezlak J, Elsaid NMH, Lin Z, Wen Q, Mustafi SM, et al. Longitudinal white-matter abnormalities in sports-related concussion: a diffusion MRI study. Neurology. 2020;95:e781–92.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Serbruyns L, Gooijers J, Caeyenberghs K, Meesen RL, Cuypers K, Sisti HM, et al. Bimanual motor deficits in older adults predicted by diffusion tensor imaging metrics of corpus callosum subregions. Brain Struct Funct. 2015;220:273–90.

    Article  CAS  PubMed  Google Scholar 

  55. Gooijers J, Swinnen SP. Interactions between brain structure and behavior: the corpus callosum and bimanual coordination. Neurosci Biobehav Rev. 2014;43:1–19.

    Article  CAS  PubMed  Google Scholar 

  56. Charney MF, Howell DR, Lanois C, Starr TC, Liao H, Coello E, et al. Associations between neurochemistry and gait performance following concussion in collegiate athletes. J Head Trauma Rehabil. 2020;35:342–53.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Dettwiler A, Murugavel M, Putukian M, Cubon V, Furtado J, Osherson D. Persistent differences in patterns of brain activation after sports-related concussion: a longitudinal functional magnetic resonance imaging study. J Neurotrauma. 2014;31:180–8.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Leech R, Sharp DJ. The role of the posterior cingulate cortex in cognition and disease. Brain. 2014;137:12–32.

    Article  PubMed  Google Scholar 

  59. Zhu FF, Maxwell JP, Hu Y, Zhang ZG, Lam WK, Poolton JM, et al. EEG activity during the verbal-cognitive stage of motor skill acquisition. Biol Psychol. 2010;84:221–7.

    Article  CAS  PubMed  Google Scholar 

  60. Shadmehr R, Holcomb HH. Neural correlates of motor memory consolidation. Science. 1997;277:821–5.

    Article  CAS  PubMed  Google Scholar 

  61. Urban KJ, Barlow KM, Jimenez JJ, Goodyear BG, Dunn JF. Functional near-infrared spectroscopy reveals reduced interhemispheric cortical communication after pediatric concussion. J Neurotrauma. 2015;32:833–40.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Helmich I, Coenen J, Henckert S, Pardalis E, Schupp S, Lausberg H. Reduced frontopolar brain activation characterizes concussed athletes with balance deficits. Neuroimage Clin. 2020;25:102164.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Helmich I, Berger A, Lausberg H. Neural control of posture in individuals with persisting postconcussion symptoms. Med Sci Sports Exerc. 2016;48:2362–9.

    Article  PubMed  Google Scholar 

  64. Helmich I, Saluja RS, Lausberg H, Kempe M, Furley P, Berger A, et al. Persistent postconcussive symptoms are accompanied by decreased functional brain oxygenation. J Neuropsychiatry Clin Neurosci. 2015;27:287–98.

    Article  PubMed  Google Scholar 

  65. Thompson J, Sebastianelli W, Slobounov S. EEG and postural correlates of mild traumatic brain injury in athletes. Neurosci Lett. 2005;377:158–63.

    Article  CAS  PubMed  Google Scholar 

  66. Thompson JWG. EEG changes and balance deficits following concussion: one piece of the puzzle. In: Slobounov S, Sebastianelli W, editors. Foundations of sport-related brain injuries. Boston: Springer; 2006. p. 341–74.

  67. Slobounov S, Sebastianelli W, Hallett M. Residual brain dysfunction observed one year post-mild traumatic brain injury: combined EEG and balance study. Clin Neurophysiol. 2012;123:1755–61.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Munia TTK, Haider A, Schneider C, Romanick M, Fazel-Rezai R. A novel EEG based spectral analysis of persistent brain function alteration in athletes with concussion history. Sci Rep. 2017;7:17221.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Diekfuss JA, Hogg JA, Grooms DR, Slutsky-Ganesh AB, Singh H, Bonnette S, et al. Can we capitalize on central nervous system plasticity in young athletes to inoculate against injury? J Sci Sport Exerc. 2020. https://doi.org/10.1007/s42978-020-00080-3.

    Article  Google Scholar 

  70. Diekfuss JA, Bonnette S, Hogg JA, Riehm C, Grooms DR, Singh H, et al. Practical training strategies to apply neuro-mechanistic motor learning principles to facilitate adaptations towards injury-resistant movement in youth. J Sci Sport Exerc. 2020.

    Article  Google Scholar 

  71. Wulf G, Lewthwaite R. Optimizing performance through intrinsic motivation and attention for learning: the OPTIMAL theory of motor learning. Psychon Bull Rev. 2016;23:1382–414.

    Article  PubMed  Google Scholar 

  72. Wulf G. Attentional focus and motor learning: A review of 15 years. Int Rev Sport Exerc Psychol. 2013;6:77–104.

    Article  Google Scholar 

  73. Diekfuss JA, Janssen JA, Slutsky AB, Berry NT, Etnier JL, Wideman L, et al. An external focus of attention is effective for balance control when sleep-deprived. Int J Exerc Sci. 2018;11:84–94.

    PubMed  PubMed Central  Google Scholar 

  74. Diekfuss JA, Rhea CK, Schmitz RJ, Grooms DR, Wilkins RW, Slutsky AB, et al. The influence of attentional focus on balance control over seven days of training. J Mot Behav. 2019;51:281–92.

    Article  PubMed  Google Scholar 

  75. Kim S-A, Ryu YU, Shin HK. The effects of different attentional focus on poststroke gait. J Exerc Rehabil. 2019;15:592–6.

    Article  PubMed  PubMed Central  Google Scholar 

  76. de Melker Worms JLA, Stins JF, van Wegen EEH, Verschueren SMP, Beek PJ, Loram ID. Effects of attentional focus on walking stability in elderly. Gait Posture. 2017;55:94–9.

    Article  PubMed  Google Scholar 

  77. Sherwood DE, Lohse KR, Healy AF. The effect of an external and internal focus of attention on dual-task performance. J Exp Psychol Hum Percept Perform. 2020;46:91–104.

    Article  PubMed  Google Scholar 

  78. Kal EC, van der Kamp J, Houdijk H. External attentional focus enhances movement automatization: a comprehensive test of the constrained action hypothesis. Hum Mov Sci. 2013;32:527–39.

    Article  CAS  PubMed  Google Scholar 

  79. Beck EN, Intzandt BN, Almeida QJ. Can dual task walking improve in Parkinson’s disease after external focus of attention exercise? A single blind randomized controlled trial. Neurorehabil Neural Repair. 2018;32:18–33.

    Article  PubMed  Google Scholar 

  80. Diekfuss JA, Grooms DR, Hogg JA, Singh H, Slutsky-Ganesh AB, Bonnette S, et al. Targeted application of motor learning theory to leverage youth neuroplasticity for enhanced injury-resistance and exercise performance: OPTIMAL PREP. J Sci Sport Exercise. 2021;3:17–36.

    Article  Google Scholar 

  81. Chiviacowsky S, Wulf G. Feedback after good trials enhances learning. Res Q Exerc Sport. 2007;78:40–7.

    Article  PubMed  Google Scholar 

  82. Zarghami M, Saemi E, Fathi I. External focus of attention enhances discus throwing performance. Kinesiology. 2012;44:47–51.

    Google Scholar 

  83. Ehlers DK, Banducci SE, Daugherty AM, Fanning J, Awick EA, Porter GC, et al. Effects of gait self-efficacy and lower-extremity physical function on dual-task performance in older adults. Biomed Res Int. 2017;2017:8570960.

    Article  PubMed  PubMed Central  Google Scholar 

  84. Liu-Ambrose T, Katarynych LA, Ashe MC, Nagamatsu LS, Hsu CL. Dual-task gait performance among community-dwelling senior women: the role of balance confidence and executive functions. J Gerontol A Biol Sci Med Sci. 2009;64:975–82.

    Article  PubMed  Google Scholar 

  85. Sakurada T, Nakajima T, Morita M, Hirai M, Watanabe E. Improved motor performance in patients with acute stroke using the optimal individual attentional strategy. Sci Rep. 2017;7:492.

    Article  CAS  Google Scholar 

  86. Schmidt RA. A schema theory of discrete motor skill learning. Psychol Rev Am Psychol Assoc. 1975;82:225–60.

    Google Scholar 

  87. Magill RA, Hall KG. A review of the contextual interference effect in motor skill acquisition. Hum Mov Sci. 1990;9:241–89.

    Article  Google Scholar 

  88. Shea JB, Morgan RL. Contextual interference effects on the acquisition, retention, and transfer of a motor skill. J Exp Psychol Hum Learn Mem. 1979;5:179–87.

    Article  Google Scholar 

  89. Schöllhorn WI, Mayer-Kress G, Newell KM, Michelbrink M. Time scales of adaptive behavior and motor learning in the presence of stochastic perturbations. Hum Mov Sci. 2009;28:319–33.

    Article  PubMed  Google Scholar 

  90. Stergiou N, Harbourne R, Cavanaugh J. Optimal movement variability: a new theoretical perspective for neurologic physical therapy. J Neurol Phys Ther. 2006;30:120–9.

    Article  PubMed  Google Scholar 

  91. Howell DR, Bonnette S, Diekfuss JA, Grooms DR, Myer GD, Wilson JC, et al. Dual-task gait stability after concussion and subsequent injury: an exploratory investigation. Sensors (Basel). 2020.

  92. Goh H-T, Sullivan KJ, Gordon J, Wulf G, Winstein CJ. Dual-task practice enhances motor learning: a preliminary investigation. Exp Brain Res. 2012;222:201–10.

    Article  PubMed  Google Scholar 

  93. Fritz NE, Cheek FM, Nichols-Larsen DS. Motor-cognitive dual-task training in persons with neurologic disorders: a systematic review. J Neurol Phys Ther. 2015;39:142–53.

    Article  PubMed  PubMed Central  Google Scholar 

  94. Pang MYC, Yang L, Ouyang H, Lam FMH, Huang M, Jehu DA. Dual-task exercise reduces cognitive-motor interference in walking and falls after stroke. Stroke. 2018;49:2990–8.

    Article  PubMed  Google Scholar 

  95. Simon JE, Millikan N, Yom J, Grooms DR. Neurocognitive challenged hops reduced functional performance relative to traditional hop testing. Phys Ther Sport. 2020;41:97–102.

    Article  PubMed  Google Scholar 

  96. Leddy JJ, Haider MN, Ellis MJ, Mannix R, Darling SR, Freitas MS, et al. Early subthreshold aerobic exercise for sport-related concussion: a randomized clinical trial. JAMA Pediatr. 2019;173:319.

    Article  PubMed  PubMed Central  Google Scholar 

  97. Haider MN, Bezherano I, Wertheimer A, Siddiqui AH, Horn EC, Willer BS, et al. Exercise for sport-related concussion and persistent postconcussive symptoms. Sports Health. 2021;13:154–60.

    Article  PubMed  Google Scholar 

  98. Howell DR, Brilliant AN, Meehan WP. Tandem gait test-retest reliability among healthy child and adolescent athletes. J Athl Train. 2019;54:1254–9.

    Article  PubMed  PubMed Central  Google Scholar 

  99. Eagle SR, Kontos AP, Pepping G-J, Johnson CD, Sinnott A, LaGoy A, et al. Increased risk of musculoskeletal injury following sport-related concussion: a perception-action coupling approach. Sports Med. 2019;50:15–23.

    Article  Google Scholar 

  100. Sandel N, Reynolds E, Cohen PE, Gillie BL, Kontos AP. Anxiety and mood clinical profile following sport-related concussion: from risk factors to treatment. Sport Exerc Perform Psychol. 2017;6:304–23.

    PubMed  PubMed Central  Google Scholar 

  101. Adkin AL, Carpenter MG. New insights on emotional contributions to human postural control. Front Neurol. 2018.

  102. Hauck LJ, Carpenter MG, Frank JS. Task-specific measures of balance efficacy, anxiety, and stability and their relationship to clinical balance performance. Gait Posture. 2008;27:676–82.

    Article  PubMed  Google Scholar 

  103. Wulf G, Landers M, Lewthwaite R, Töllner T. External focus instructions reduce postural instability in individuals with Parkinson disease. Phys Ther. 2009;89:162–8.

    Article  PubMed  Google Scholar 

  104. Maurer H, Munzert J. Influence of attentional focus on skilled motor performance: performance decrement under unfamiliar focus conditions. Hum Mov Sci. 2013;32:730–40.

    Article  PubMed  Google Scholar 

  105. Bahmani M, Babak M, Land WM, Howard JT, Diekfuss JA, Abdollahipour R. Children’s motor imagery modality dominance modulates the role of attentional focus in motor skill learning. Hum Mov Sci. 2021;75:102742.

    Article  PubMed  Google Scholar 

  106. Sakurada T, Hirai M, Watanabe E. Optimization of a motor learning attention-directing strategy based on an individual’s motor imagery ability. Exp Brain Res. 2016;234:301–11.

    Article  PubMed  Google Scholar 

  107. Kal E, Ellmers T, Diekfuss J, Winters M, van der Kamp J. Explicit motor learning interventions are still relevant for ACL injury rehabilitation: do not put all your eggs in the implicit basket. Br J Sports Med. 2021. https://doi.org/10.1136/bjsports-2020-103643.

    Article  PubMed  Google Scholar 

  108. Makaruk H, Porter JM, Bodasińska A, Palmer S. Optimizing the penalty kick under external focus of attention and autonomy support instructions. Eur J Sport Sci. 2020;20(10):1378–86.

    Article  PubMed  Google Scholar 

  109. Pascua LAM, Wulf G, Lewthwaite R. Additive benefits of external focus and enhanced performance expectancy for motor learning. J Sports Sci. 2015;33:58–66.

    Article  PubMed  Google Scholar 

  110. Wulf G, Lewthwaite R, Cardozo P, Chiviacowsky S. Triple play: Additive contributions of enhanced expectancies, autonomy support, and external attentional focus to motor learning. Quart J Exp Psychol. 2018;71:824–31.

    Article  Google Scholar 

  111. Fraser EE, Downing MG, Biernacki K, McKenzie DP, Ponsford JL. Cognitive reserve and age predict cognitive recovery after mild to severe traumatic brain injury. J Neurotrauma. 2019;36:2753–61.

    Article  PubMed  Google Scholar 

  112. Steward KA, Kennedy R, Novack TA, Crowe M, Marson DC, Triebel KL. The role of cognitive reserve in recovery from traumatic brain injury. J Head Trauma Rehabil. 2018;33:E18-27.

    Article  PubMed  PubMed Central  Google Scholar 

  113. Kesler SR, Adams HF, Blasey CM, Bigler ED. Premorbid intellectual functioning, education, and brain size in traumatic brain injury: an investigation of the cognitive reserve hypothesis. Appl Neuropsychol. 2003;10:153–62.

    Article  PubMed  Google Scholar 

  114. Leary JB, Kim GY, Bradley CL, Hussain UZ, Sacco M, Bernad M, et al. The association of cognitive reserve in chronic-phase functional and neuropsychological outcomes following traumatic brain injury. J Head Trauma Rehabil. 2018;33:E28-35.

    Article  PubMed  PubMed Central  Google Scholar 

  115. García-Molina A, Enseñat-Cantallops A, Sánchez-Carrión R, Rodríguez P, Tormos JM, Roig-Rovira T. Interindividual variability in recovery after traumatic brain injury: effect of cognitive reserve. Med Clin (Barc). 2013;140:527–31.

    Article  Google Scholar 

  116. De Beaumont L, Henry LC, Gosselin N. Long-term functional alterations in sports concussion. Neurosurg Focus. 2012;33(E8):1–7.

    Google Scholar 

  117. Oldenburg C, Lundin A, Edman G, Nygren-de Boussard C, Bartfai A. Cognitive reserve and persistent post-concussion symptoms—a prospective mild traumatic brain injury (mTBI) cohort study. Brain Inj. 2016;30:146–55.

    Article  PubMed  Google Scholar 

  118. Stenberg J, Håberg AK, Follestad T, Olsen A, Iverson GL, Terry DP, et al. Cognitive reserve moderates cognitive outcome after mild traumatic brain injury. Arch Phys Med Rehabil. 2020;101:72–80.

    Article  PubMed  Google Scholar 

  119. Tucker-Drob EM, Johnson KE, Jones RN. The cognitive reserve hypothesis: a longitudinal examination of age-associated declines in reasoning and processing speed. Dev Psychol. 2009;45:431–46.

    Article  PubMed  PubMed Central  Google Scholar 

  120. Stern Y. Cognitive reserve in ageing and Alzheimer’s disease. Lancet Neurol. 2012;11:1006–12.

    Article  PubMed  PubMed Central  Google Scholar 

  121. Stern Y. Cognitive reserve. Neuropsychologia. 2009;47:2015–28.

    Article  PubMed  PubMed Central  Google Scholar 

  122. Howell DR, Osternig LR, Chou L-S. Detection of acute and long-term effects of concussion: dual-task gait balance control versus computerized neurocognitive test. Arch Phys Med Rehabil. 2018;99:1318–24.

    Article  PubMed  Google Scholar 

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Correspondence to Jason M. Avedesian.

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Jason M. Avedesian, Harjiv Singh, Jed A. Diekfuss, Gregory D. Myer, and Dustin R. Grooms declare they have no conflicts of interest relevant to the content of this review.

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Avedesian, J.M., Singh, H., Diekfuss, J.A. et al. Loss of Motor Stability After Sports-Related Concussion: Opportunities for Motor Learning Strategies to Reduce Musculoskeletal Injury Risk. Sports Med 51, 2299–2309 (2021). https://doi.org/10.1007/s40279-021-01527-5

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