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Research Article

Cortical and cerebellar structural correlates of cognitive-motor integration performance in females with and without persistent concussion symptoms

, , , & ORCID Icon
Pages 397-411 | Received 24 May 2022, Accepted 16 Nov 2022, Published online: 22 Dec 2022

References

  • Centers for Disease Control and Prevention (CDC). Nonfatal traumatic brain injuries from sports and recreation activities — united States, 2001-2005. Morb Mortal Wkly Rep. 2007;56(29):733–37.
  • Harmon KG, Drezner JA, Gammons M, Guskiewicz M, Halstead M, Herring SA, Kutcher JS, Pana A, Putukian M, Roberts WO. American medical society for sports medicine position statement: concussion in sport. Br J Sports Med. 2013;47(1):15–26.doi:10.1136/bjsports-2012-091941.
  • McCrory P, Meeuwisse W, Dvorak J, Aubry M, Bailes J, Broglio S, Cantu RC, Cassidy D, Echemendia RJ, Castellani RJ, 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(11):838–47.doi:10.1136/bjsports-2017-097699.
  • World Health Organization (WHO). The ICD-10 classification of mental and behavioural disorders. Genève, Switxerland; 1992. 67–68p.
  • American Psychiatric Association. Diagnostic and statistical manual of mental disorders. Washington DC: IV-TR; 2000. p. 760–62.
  • Tator CH, Davis HS, Dufort PA, Tartaglia MC, Davis KD, Ebraheem A, Hiploylee C. Postconcussion syndrome: demographics and predictors in 221 patients. J Neurosurg. 2016;125(5):1206–16.doi:10.3171/2015.6.JNS15664.
  • Hiploylee C, Dufort PA, Davis HS, Wennberg RA, Tartaglia MC, Mikulis D, Hazrati L-N, Tator C. Longitudinal study of postconcussion syndrome: not everyone recovers. J Neurotrauma. 2017;34(8):1511–23.doi:10.1089/neu.2016.4677.
  • National Center for Injury Prevention and Control. Report to congress on mild traumatic brain injury in the United States: steps to prevent a serious public health problem. Atlanta, GA: Centers for Disease Control and Prevention; 2003.
  • Evans RW. Persistent post-traumatic headache, postconcussion syndrome, and whiplash injuries: the evidence for a non-traumatic basis with an historical review. Headache. 2010;50(4):716–24.doi:10.1111/j.1526-4610.2010.01645.x.
  • Ryan LM, Warden DL. Post concussion syndrome. Int Rev Psychiatry. 2003;15(4):310–16.doi:10.1080/09540260310001606692.
  • Silverberg ND, Iverson GL. Etiology of the post-concussion syndrome: physiogenesis and psychogenesis revisited. NeuroRehabilitation. 2011;29(4):317–29.doi:10.3233/NRE-2011-0708.
  • Bigler ED. Neuropsychology and clinical neuroscience of persistent post-concussive syndrome. J Int Neuropsychol Soc. 2008;14(1):1–22.doi:10.1017/S135561770808017X.
  • Giza CC, Hovda DA. The new neurometabloic cascade of concussion. Neurosurgery. 2015;75(Supplement 4):S24–33.doi:10.1227/NEU.0000000000000505.
  • Warner MA, Youn TS, Davis T, Chandra A, Marquez de la Plata C, Moore C, Harper C, Madden CJ, Spence J, McColl R, et al. Regionally selective atrophy after traumatic axonal injury. Arch Neurol. 2010;67(11):1336–44.doi:10.1001/archneurol.2010.149.
  • Urban K, Riggs L, Wells G, Keightley M, Chen J-K, Ptito A, Fait P, Taha T, Sinopoli KJ. Cortical thickness changes and thier relationship to dual-task performance following mild traumatic brain injury in youth. J Neurotrauma. 2017;34(4):816–23.doi:10.1089/neu.2016.4502.
  • Sussman D, Chakravarty MM, Pang EW, Taylor MJ, Dunkley BT, Dunkley BT. Concussion induces focal and widespread neuromorphological changes. Neurosci Lett. 2017;650:52–59.doi:10.1016/j.neulet.2017.04.026.
  • Hayes JP, Logue MW, Sadeh N, Spielberg JM, Verfaellie M, Hayes SM, Reagan A, Salat DH, Wolf EJ, McGlinchey RE, et al. Mild traumatic brain injury is associated with reduced cortical thickness in those at risk for Alzheimer’s disease. Brain. 2017;140(3):813–25.doi:10.1093/brain/aww344.
  • Zhou Y, Kierans A, Kenul D, Ge Y, Rath J, Reaume J, Grossman RI, Lui YW. Mild traumatic brain injury: longitudinal regional brain volume changes. Radiology. 2013;267(3):880–90.doi:10.1148/radiol.13122542.
  • Govindarajan KA, Narayana PA, Hasan KM, Wilde EA, Levin HS, Hunter JV, Miller ER, Patel VKS, Robertson CS, McCarthy JJ. Cortical thickness in mild traumatic brain injury. J Neurotrauma. 2016;33(20):1809–17.doi:10.1089/neu.2015.4253.
  • Zivanovic N, Virani S, Rajaram AA, Lebel C, Yeates KO, Brooks BL. Cortical volume and thickness in youth several years after concussion. J Child Neurol. 2021;36(3):186–94.doi:10.1177/0883073820962930.
  • Spanos GK, Wilde EA, Bigler ED, Cleavinger HB, Fearing MA, Levin HS, Levin HS, Li X, Hunter JV. Cerebellar atrophy after moderate-tosevere pediatric traumatic brain injury. Am J Neuroradiol. 2007;28(3):537–42.
  • Kan E, Ling E, Lu J. Long term manifestation of cerebellar biochemical, histopathological and functional changes after mild and severe fluid percussion injury in rodents. In: Neuroscience Meeting Planner.Society for Neuroscience Conference; 2013 Nov 9-13; San Diego CA.
  • Meabon JS, Huber BR, Cross DJ, Richards TL, Minoshima S, Pagulayan KF, Meeker KD, Kraemer BC, Petrie EC, Raskine MA, et al. Repetitive blast exposure in mice and combat veterans causes persistent cerebellar dysfunction. Sci Transl Med. 2016;8(321):1–16.doi:10.1126/scitranslmed.aaa9585.
  • Ross DE, Ochs AL, Seabaugh JM, DeMark MF, Shrader CR, Marwitz JH, Havranek MD. Progressive brain atrophy in patients with chronic neuropsychiatric symptoms after mild traumatic brain injury: a preliminary study. Brain Inj. 2012;26(12):1500–09.doi:10.3109/02699052.2012.694570.
  • Wise SP, Boussaoud D, Johnson PB, Caminiti R. Premotor and parietal cortex: corticocortical connectivity and combinatorial computations. Annu Rev Neurosci. 1997;20(1):25–42.doi:10.1146/annurev.neuro.20.1.25.
  • Sabes PN. The planning and control of reaching movements. Curr Opin Neurobiol. 2000;10(6):740–46.doi:10.1016/S0959-4388(00)00149-5.
  • Kandel ER, Schwartz JH, Jessell TM, Siegelbaum SA, Hudspeth A, editors. Principles of Neural Science. 5th ed. New York (NY): McGraw-Hill; 2000.
  • Sergio L, Gorbet D, Tippett W, Yan X, Neagu B. When what you see isn’t where you get: cortical mechanisms of vision for complex action. In: Jenkin M, Harris L, editors. Cortical mechanisms of vision. Cambridge (UK): Cambridge University Press; 2009. p. 81–118.
  • Wise S, Di Pellegrino G, Boussaoud D. The premotor cortex and nonstandard sensorimotor mapping. Can J Physiol Pharmacol. 1996;74(4):469–82.doi:10.1139/cjpp-74-4-469.
  • Dalecki M, Albines D, Macpherson A, Sergio LE. Prolonged cognitive–motor impairments in children and adolescents with a history of concussion. Concussion. 2016;1(3):CNC14.doi:10.2217/cnc-2016-0001.
  • Brown J, Dalecki M, Hughes C, Macpherson AK, Sergio LE. Cognitive-motor integration deficits in young adult athletes following concussion. BMC Sports Sci Med Rehabil. 2015;7(25). doi:10.1186/s13102-015-0019-4.
  • Hurtubise J, Gorbet D, Hamandi Y, Macpherson A, Sergio L. The effect of concussion history on cognitive-motor integration in elite hockey players. Concussion. 2016;1(3):CNC17.doi:10.2217/cnc-2016-0006.
  • McCrory P, Meeuwisse WH, Aubry M, Cantu B, Dvořák J, Echemendia RJ, Engebretsen L, Johnston K, Kutcher JS, Raftery M, et al. Consensus statement on concussion in sport: the 4th international conference on concussion in sport held in Zurich, november 2012. Br J Sports Med. 2013;47(5):250–58.doi:10.1136/bjsports-2013-092313.
  • Song M-K, Lin F-C, Ward SE, Fine JP. Composite variables: when and how. Nurs Res. 2013;62(1):45–49.doi:10.1097/NNR.0b013e3182741948.
  • Fischl B. FreeSurfer. Neuroimage. 2012;62(2):774–81.doi:10.1016/j.neuroimage.2012.01.021.
  • Fischl B, Dale A. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci. 2000;97(20):11050–55.doi:10.1073/pnas.200033797.
  • Cardinale F, Chinnici G, Bramerio M, Mai R, Sartori I, Cossu M, Lo Russo G, Castana L, Colombo N, Caborni C, et al. Validation of FreeSurfer-estimated brain cortical thickness: comparison with histologic measurements. Neuroinformatics. 2014;12(4):535–42.doi:10.1007/s12021-014-9229-2.
  • Rosas HD, Liu AK, Hersch S, Glessner M, Ferrante RJ, Salat DH, van der Kouwe A, Jenkins BG, Dale AM, Fischl B. Regional and progressive thinning of the cortical ribbon in Huntington’s disease. Neurology. 2002;58(5):695–701.doi:10.1212/WNL.58.5.695.
  • Han X, Jovicich J, Salat D, van der Kouwe A, Quinn B, Czanner S, Busa E, Pacheco J, Albert M, Killinay R, et al. Reliability of MRI-derived measurements of human cerebral cortical thickness: the effects of field strength, scanner upgrade and manufacturer. Neuroimage. 2006;32(1):180–94.doi:10.1016/j.neuroimage.2006.02.051.
  • Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM. FSL. Neuroimage. 2012;62(2):782–90.doi:10.1016/j.neuroimage.2011.09.015.
  • Tudorascu DL, Karim HT, Maronge JM, Alhilali L, Fakhran S, Aizenstein HJ, Muschelli J, Crainiceanu CM. Reproducibility and bias in healthy brain segmentation: comparison of two popular neuroimaging platforms. Front Neurosci. 2016;10:1–8.doi:10.3389/fnins.2016.00503.
  • Pérez ARP Accurate segmentation of brain MR images [ thesis]. Göteborg (Sweden): Chalmers University of Technology; 2010.
  • Smith SM. Fast robust automated brain extraction. Hum Brain Mapp. 2002;17(3):143–55.doi:10.1002/hbm.10062.
  • Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 2002;17(2):825–41.doi:10.1006/nimg.2002.1132.
  • Zhang Y, Smith S, Brady M. Segmentation of brain MR images through a hidden markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imaging. 2001;20(1):45–57.doi:10.1109/42.906424.
  • Greve DN, Fischl B. False positive rates in surface-based anatomical analysis. Neuroimage. 2018;171:6–14.doi:10.1016/j.neuroimage.2017.12.072.
  • Hagler DJ, Saygin AP, Sereno MI. Smoothing and cluster thresholding for cortical surface-based group analysis of fMRI data. Neuroimage. 2006;33(4):1093–103.doi:10.1016/j.neuroimage.2006.07.036.
  • Gorbet DJ, Staines WR, Sergio LE. Brain mechanisms for preparing increasingly complex sensory to motor transformations. Neuroimage. 2004;23(3):1100–11.doi:10.1016/j.neuroimage.2004.07.043.
  • Granek JA, Sergio LE. Evidence for distinct brain networks in the control of rule-based motor behavior. J Neurophysiol. 2015;114(2):1298–309.doi:10.1152/jn.00233.2014.
  • Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage. 2006;31(3):968–80.doi:10.1016/j.neuroimage.2006.01.021.
  • Diedrichsen J. A spatially unbiased atlas template of the human cerebellum. Neuroimage. 2006;33(1):127–38.doi:10.1016/j.neuroimage.2006.05.056.
  • Diedrichsen J, Balsters JH, Flavell J, Cussans E, Ramnani N. A probabilistic MR atlas of the human cerebellum. Neuroimage. 2009;46(1):39–46.doi:10.1016/j.neuroimage.2009.01.045.
  • Albaugh MD, Orr C, Nickerson JP, Zweber C, Slauterbeck JR, Hipko S, Gonyea J, Andrews T, Brackenbury JC, Watts R, et al. Postconcussion symptoms are associated with cerebral cortical thickness in healthy collegiate and preparatory school ice hockey players. J Pediatr. 2015;166(2):394–400.doi:10.1016/j.jpeds.2014.10.016.
  • Wang X, Xie H, Cotton AS, Tamburrino MB, Brickman KR, Lewis TJ, McLean SA, Liberzon I. Early cortical thickness change after mild traumatic brain injury following motor vehicle collision. J Neurotrauma. 2015;32(7):455–63.doi:10.1089/neu.2014.3492.
  • Ware AL, Goodrich-Hunsaker NJ, Lebel C, Shukla A, Wilde EA, Abildskov TJ, Biger ED, Cohen DM, Mihalov LK, Bacevice A, et al. Post-acute cortical thickness in children with mild traumatic brain injury versus orthopedic injury. J Neurotrauma. 2020;37(17):1892–901.doi:10.1089/neu.2019.6850.
  • Grieve SM, Korgaonkar MS, Koslow SH, Gordon E, Williams LM. Widespread reductions in gray matter volume in depression. NeuroImage Clin. 2013;3:332–39.doi:10.1016/j.nicl.2013.08.016.
  • Szymkowicz SM, McLaren ME, Kirton JW, O’Shea A, Woods AJ, Manini TM, Anton SD, Dotson VM. Depressive symptom severity is associated with increased cortical thickness in older adults. Int J Geriatr Psychiatry. 2016;31(4):325–33.doi:10.1002/gps.4324.
  • Brühl AB, Hänggi J, Baur V, Rufer M, Delsignore A, Weidt S, Jäncke L, Herwig U. Increased cortical thickness in a frontoparietal network in social anxiety disorder. Hum Brain Mapp. 2014;35(7):2966–77.doi:10.1002/hbm.22378.
  • Wilde EA, Newsome MR, Bigler ED, Pertab J, Merkley TL, Hanten G, Scheibel RS, Li X, Chu Z, Yallampalli R, et al. Brain imaging correlates of verbal working memory in children following traumatic brain injury. Int J Psychophysiol 2011;82:86–96.
  • McCrea M, Meier T, Huber D, Ptito A, Bigler E, Debert CT, Manley G, Menon D, Chen J-K, Wall R, et al. Role of advanced neuroimaging, fluid biomarkers and genetic testing in the assessment of sport-related concussion: a systematic review. Br J Sports Med. 2017;51(12):919–29.doi:10.1136/bjsports-2016-097447.
  • Esopenko C, Kumar P, Alain C, Chow T, McIntosh A, Strother S, Levine B. Neuroimaging during a working memory task in remote traumatic brain injury: evidence from NHL alumni. In: 20th Annual Meeting of the Cognitive Neuroscience Society; 2013 April; B60. San Francisco, California.
  • Chamard E, Lichtenstein JD. A systematic review of neuroimaging findings in children and adolescents with sports-related concussion. Brain Inj. 2018;9052:1–16.
  • Chen JK, Johnston KM, Frey S, Petrides M, Worsley K, Ptito A. Functional abnormalities in symptomatic concussed athletes: an fMRI study. Neuroimage. 2004;22(1):68–82.doi:10.1016/j.neuroimage.2003.12.032.
  • Chen JK, 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(11):1231–38.doi:10.1136/jnnp.2006.110395.
  • Bodranghien F, Bastian A, Casali C, Hallett M, Louis ED, Manto M, Mariën P, Nowak DA, Schmahmann JD, Serrao M, et al. Consensus paper: revisiting the symptoms and signs of cerebellar syndrome. Cerebellum. 2016;15(3):369–91.doi:10.1007/s12311-015-0687-3.
  • Roostaei T, Nazeri A, Sahraian MA, Minagar A. The human cerebellum: a review of physiologic neuroanatomy. Neurol Clin. 2014;32(4):859–69.doi:10.1016/j.ncl.2014.07.013.
  • Yorke AM, Smith L, Babcock M, Alsalaheen B. Validity and reliability of the vestibular/ocular motor screening and associations with common concussion screening tools. Sports Health. 2017;9(2):174–80.doi:10.1177/1941738116678411.
  • Corwin DJ, Wiebe DJ, Zonfrillo MR, Grady MF, Robinson RL, Goodman AM, Master CL. Vestibular deficits following youth concussion. J Pediatr. 2015;166(5):1221–25.doi:10.1016/j.jpeds.2015.01.039.
  • Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage. 2009;44(2):489–501.doi:10.1016/j.neuroimage.2008.08.039.
  • Xue A, Kong R, Yang Q, Eldaief MC, Angeli PA, DiNicola LM, Braga RM, Bucker RL, Yeo BTT. The detailed organization of the human cerebellum estimated by intrinsic functional connectivity within the individual. J Neurophysiol. 2021;125(125):358–84.doi:10.1152/jn.00561.2020.
  • Stoodley CJ. The cerebellum and cognition: evidence from functional imaging studies. Cerebellum. 2012;11(2):352–65.doi:10.1007/s12311-011-0260-7.
  • Stoodley CJ, Schmahmann JD. Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex. 2010;46(7):831–44.doi:10.1016/j.cortex.2009.11.008.
  • Grodd W, Hülsmann E, Lotze M, Wildgruber D, Erb M. Sensorimotor mapping of the human cerebellum: fMRI evidence of somatotopic organization. Hum Brain Mapp. 2001;13(2):55–73.doi:10.1002/hbm.1025.
  • Krienen FM, Buckner RL. Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity. Cereb Cortex. 2009;19(10):2485–97.doi:10.1093/cercor/bhp135.
  • Ivry RB, Keele SW. Timing functions of the cerebellum. J Cogn Neurosci. 1989;1(2):136–52.doi:10.1162/jocn.1989.1.2.136.
  • Ivry RB, Keele SW, Diener HC. Dissociation of the lateral and medial cerebellum in movement timing and movement execution. Exp Brain Res. 1988;73(1):167–80.doi:10.1007/BF00279670.
  • Clower D, Boussaoud D. Selective use of perceptual recalibration versus visuomotor skill acquisition. J Neurophysiol. 2000;84(5):2703–08.doi:10.1152/jn.2000.84.5.2703.
  • Redding GM, Wallace B. Adaptive spatial alignment and strategic perceptual-motor control. J Exp Psychol Hum Percept Perform. 1996 Apr;22(2):379–94. doi:10.1037/0096-1523.22.2.379.
  • Granek JA, Pisella L, Stemberger J, Vighetto A, Rossetti Y, Sergio L, Balasubramaniam R. Decoupled visually-guided reaching in optic ataxia: differences in motor control between canonical and non-canonical orientations in space. PLoS One. 2013;8(12):e86138.doi:10.1371/journal.pone.0086138.
  • Granek JA, Pisella L, Blangero A, Rossetti Y, Sergio LE, Balasubramaniam R. The role of the caudal superior parietal lobule in updating hand location in peripheral vision: further evidence from optic ataxia. PLoS One. 2012;7(10):e46619.doi:10.1371/journal.pone.0046619.
  • Hawkins KM, Sayegh P, Yan X, Crawford JD, Sergio LE. Neural actvity in superior parietal cortex during rule-based visual-motor transformations. J Cogn Neurosci. 2013;25(3):436–54.doi:10.1162/jocn_a_00318.
  • Sayegh PF, Hawkins KM, Hoffman KL, Sergio LE. Differences in spectral profiles between rostral and caudal premotor cortex when hand-eye actions are decoupled. J Neurophysiol. 2013;110(4):952–63.doi:10.1152/jn.00764.2012.
  • Sayegh PF, Gorbet DJ, Hawkins KM, Hoffman KL, Sergio LE. The contribution of different cortical regions to the control of spatially decoupled eye–hand coordination. J Cogn Neurosci. 2017;29(7):1194–211.
  • Miller EK, Cohen JD. An integrative theory of prefrontal cortex function. Annu Rev Neurosci. 2001;24(1):167–202.doi:10.1146/annurev.neuro.24.1.167.
  • Husain M, Nachev P. Space and the parietal cortex. Trends Cogn Sci. 2007;11(1):30–36.doi:10.1016/j.tics.2006.10.011.
  • Huddleston WE, DeYoe EA. The representation of spatial attention in human parietal cortex dynamically modulates with performance. Cereb Cortex. 2008;18(6):1272–80.doi:10.1093/cercor/bhm158.
  • Clower DM, West RA, Lynch JC, Strick PL. The inferior parietal lobule is the target of output from the superior colliculus, hippocampus, and cerebellum. J Neurosci. 2001;21(16):6283–91.doi:10.1523/JNEUROSCI.21-16-06283.2001.
  • Gorbet DJ, Sergio LE. Don’t watch where you’re going: the neural correlates of decoupling eye and arm movements. Behav Brain Res. 2016;298:229–40.doi:10.1016/j.bbr.2015.11.012.
  • Granek JA, Gorbet D, Sergio L. Extensive video-game experience alters cortical networks for complex visuomotor transformations. Cortex. 2010;46(9):1165–77.doi:10.1016/j.cortex.2009.10.009.
  • Cavanna AE, Trimble MR. The precuneus: a review of its functional anatomy and behavioural correlates. Brain. 2006;129(Pt 3):564–83.doi:10.1093/brain/awl004.
  • Gorbet DJ, Sergio LE. Looking up while reaching out: the neural correlates of making eye and arm movements in different spatial planes. Exp Brain Res. 2019;237(1):57–70.doi:10.1007/s00221-018-5395-z.
  • Churchill N, Hutchison MG, Leung G, Graham S, Schweizer TA. Changes in functional connectivity of the brain associated with a history of sport concussion: a preliminary investigation. Brain Inj. 2017;31(1):39–48.doi:10.1080/02699052.2016.1221135.