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Functional abnormalities in normally appearing athletes following mild traumatic brain injury: a functional MRI study

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Abstract

Memory problems are one of the most common symptoms of sport-related mild traumatic brain injury (MTBI), known as concussion. Surprisingly, little research has examined spatial memory in concussed athletes given its importance in athletic environments. Here, we combine functional magnetic resonance imaging (fMRI) with a virtual reality (VR) paradigm designed to investigate the possibility of residual functional deficits in recently concussed but asymptomatic individuals. Specifically, we report performance of spatial memory navigation tasks in a VR environment and fMRI data in 15 athletes suffering from MTBI and 15 neurologically normal, athletically active age matched controls. No differences in performance were observed between these two groups of subjects in terms of success rate (94 and 92%) and time to complete the spatial memory navigation tasks (mean = 19.5 and 19.7 s). Whole brain analysis revealed that similar brain activation patterns were observed during both encoding and retrieval among the groups. However, concussed athletes showed larger cortical networks with additional increases in activity outside of the shared region of interest (ROI) during encoding. Quantitative analysis of blood oxygen level dependent (BOLD) signal revealed that concussed individuals had a significantly larger cluster size during encoding at parietal cortex, right dorsolateral prefrontal cortex, and right hippocampus. In addition, there was a significantly larger BOLD signal percent change at the right hippocampus. Neither cluster size nor BOLD signal percent change at shared ROIs was different between groups during retrieval. These major findings are discussed with respect to current hypotheses regarding the neural mechanism responsible for alteration of brain functions in a clinical setting.

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References

  • Audoin B, Ibarrola D, Ranjeva JP, Confort-Gouny S, Malikova I, Ali-Cherif A, Pelletier J, Cozzone P (2003) Compensatory cortical activation observed by fMRI during a cognitive task at the earliest stage of MS. Hum Brain Mapp 20:51–58

    Article  PubMed  Google Scholar 

  • Bluml S, Brooks W (2006) Magnetic resonance spectroscopy of traumatic brain injury and concussion. In: Slobounov S, Sebastianelli W (eds) Foundations of sport-related brain injuries. Spinger, NY, pp 197–220

    Chapter  Google Scholar 

  • Brett M, Anton J-L, Valabregue R, Poline J-B (2002) Region of interest analysis using an SPM toolbox [abstract]. Presented at the 8th International Conference on Functional Mapping of the Human Brain, 2–6 June, Sendai, Japan. Available on CD-ROM in Neuroimage 16(2)

  • Bryant R, Harvey A (1999) Postconcussive symptoms and posttraumatic stress disorder after mind traumatic brain injury. J Nerv Ment Dis 187:302–305

    Article  CAS  PubMed  Google Scholar 

  • Burgess N, Maguire A, O’Keefe J (2002) The human hippocampus and spatial and episodic memory. Neuron 35:625–641

    Article  CAS  PubMed  Google Scholar 

  • Cantu R (2006) Concussion classification: ongoing controversy. In: Slobounov S, Sebastianelli W (eds) Foundations of sport-related brain injuries. Springer, NY, pp 87–111

    Chapter  Google Scholar 

  • Cao C, Slobounov S (2009) Alteration of cortical functional connectivity as a result of traumatic brain injury revealed by graph theory, ICA and sLORETA analyses of EEG signals. IEEE (in press)

  • Chen JK, Johnston KM, Frey S, Petrides M, Worsley K, Ptito A (2004) Functional abnormalities in symptomatic concussed athletes: an fMRI study. Neuroimage 22:68–82

    Article  PubMed  Google Scholar 

  • Chen J-K, Johnston K, Collie A, McCrory P, Ptito A (2007) A validation of the post concussion symptom scale in the assessment of complex concussion using cognitive testing and functional MRI. J Neurosurg Psychiatry 78:1231–1238

    Article  Google Scholar 

  • Chiaravalloti N, Hillary F, Ricker J, Christodoulou C, Kalnin A, Liu WC et al (2005) Cerebral activation patterns during working memory performance in multiple sclerosis using fMRI. J Clin Exp Neuropsychol 27(1):33–54

    Article  PubMed  Google Scholar 

  • Curtis C, D’Esposito M (2003) Persistent activity in the prefrontal cortex during working memory. Trends Cogn Sci 7:415–423

    Article  PubMed  Google Scholar 

  • Daselaar S, Prince S, Dennis N, Hayes S, Kim H, Cabeza R (2009) Posterior midline and ventral parietal activity is associated with retrieval success and encoding failure. Front Hum Neurosci 3:1–10

    Article  Google Scholar 

  • Dennis N, Cabeza R (2007) Neuroimaging of healthy cognitive aging. In: Craik F, Salthouse T (eds) The handbook of aging and cognition, 3rd edn. Psychology Press, New York

    Google Scholar 

  • Friston KJ, Holmes AP, Worsley KJ, POline J-P, Frithh CD, Frackowiak RSJ (1995) Statistical parametric maps in functional neuroimaging. A general linear approach. Hum Brain Mapp 2:189–210

    Article  Google Scholar 

  • Garnett MR, Blamire AM, Corkill RG et al (2000) Early proton magnetic resonance spectroscopy in normal-appearing brain correlates with outcome in patients following traumatic brain injury. Brain 123:2040–2054

    Article  Google Scholar 

  • Garnett MR, Corkill RG, Blamire AM et al (2001) Altered cellular metabolism following traumatic brain injury: a magnetic resonance spectroscopy study. J Neurotrauma 18:231–240

    Article  CAS  PubMed  Google Scholar 

  • Guskiewicz K (2003) Assessment of postural stability following sport-related concussion. Curr Sport Med Rep 2(1):24–30

    Google Scholar 

  • Guskiewicz K, Mihalik J (2006) The biomechanics and pathomechanics of sport-related concussion: looking at history to build the future. In: Slobounov S, Sebastianelli W (eds) Foundations of sport-related brain injuries. Springer, NY, pp 65–84

    Chapter  Google Scholar 

  • Hartley T, Maguire E, Spiers H, Burgess N (2003) The well-worn route and the path less traveled: distinct neural bases of route following and wayfinding in humans. Neuron 37:877–888

    Article  CAS  PubMed  Google Scholar 

  • Hayes S, Ryan L, Schnyer D, Nadel L (2004) An fMRI study of episodic memory: retrieval of object, spatial and temporal information. Behav Neurosci 118:885–896

    Article  PubMed  Google Scholar 

  • Hillary FG (2008) Neuroimaging of working memory dysfunction and the dilemma with brain reorganization hypotheses. J Int Neuropsychol Soc 14(4):526–534

    Article  PubMed  Google Scholar 

  • Hillary FG, Chiaravalloti ND, Ricker JH, Steffener J, Bly BM, Lange G et al (2003) An investigation of working memory rehearsal in multiple sclerosis using fMRI. J Clin Exp Neuropsychol 25(7):965–978

    Article  CAS  PubMed  Google Scholar 

  • Hillary FG, Genova HM, Chiaravalloti ND, DeLuca J (2006) Prefrontal modulation of working memory performance in brain injury and disease. Hum Brain Mapp 27:837–847

    Article  PubMed  Google Scholar 

  • Iaria G, Chen J, Guariglia C, Ptito A, Petrides M (2007) Retrosplenial and hippocampal brain regions in human navigation: complementary functional contributions to the formation and use of cognitive maps. Eur J Neurosci 25:890–899

    Article  PubMed  Google Scholar 

  • Jancke L, Cheetham M, Baumgartner T (2009) Virtual reality on the role or prefrontal cortex in adults and children. Front Neurosci 3(1):52–59

    Article  PubMed  Google Scholar 

  • Jantzen KL, Anderson B, Steinberg FL et al (2004) A prospective functional MR imaging study of mild traumatic brain injury in collegiate football players. Am J Neuroradiol 25:738–745

    PubMed  Google Scholar 

  • Janzen G, Weststeijn C (2007) Neural representation of object location and route direction: an evernt-related fMRI study. Brain Res 1165:116–125

    Article  CAS  PubMed  Google Scholar 

  • Kessels R, Pastma A, Wijnalda E, Haan E (2000a) Frontal-lobe involvement in spatial memory: evidence from PET, fMRI, and lesion studies. Neuropsych Rev 10:101–113

    Article  CAS  Google Scholar 

  • Kessels RPC, de Haan EHF, Kapelle LJ, Postma A (2000b) Varieties of human spatial; memory: a meta-analysis of the effects of hippocampal lesions. Brain Res Rev 10:295–303

    Google Scholar 

  • Kirov I, Fleysher L, Babb JS, Silver JM, Grossman RI, Gonen O (2007) Characterizing ‘mild’ in traumatic brain injury with proton MR spectroscopy in the thalamus: initial findings. Brain Inj 21(11):1147–1154

    Article  PubMed  Google Scholar 

  • Lovell M, Collins M, Iverson G, Field M, Maroon J, Cantu R, Rodell K, Powell J, Fu F (2003) Recovery from concussion in high school athletes. J Neurosurg 98:296–301

    Article  PubMed  Google Scholar 

  • Lovell MR, Pardini JE, Welling J, Collins MW, Bakal J, Lazar N, Roush R, Eddy WF, Becker JT (2007) Functional brain abnormalities are related to clinical recovery and time to return-to-play in athletes. Neurosurgery 61(2):359–360

    Google Scholar 

  • Maldjian JA, Laurienti PJ, Burdette JB, Kraft RA (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19:1233–1239

    Google Scholar 

  • McAllister TW, Saykin AJ, Flashman LA et al (1999) Brain activation during working memory I month after mild traumatic brain injury: a functional MRI study. Neurology 53:1300–1308

    CAS  PubMed  Google Scholar 

  • McAllister TW, Sparling MB, Flashman LA, Guerin SJ, Mamourian AC, Saykin AJ (2001) Differential working memory load effects after mild traumatic brain injury. Neuroimage 14(5):1004–1012

    Article  CAS  PubMed  Google Scholar 

  • McAllister TW, Flashman LA, McDonald BC, Saykin AJ (2006) Mechanisms of working memory dysfunction after mild and moderate TBI: evidence from functional MRI and neurogenetics. J Neurotrauma 23:1450–1467

    Article  PubMed  Google Scholar 

  • McCrory P, Meeuwisse W, Johnston K, Dvorak J, Aubry M, Molloy M, Cantu R (2009) Consensus statement on concussion sport: the 3rd international conference on concussion in sport. Br J Sport Med 43:176–184

    Article  Google Scholar 

  • McNamara T, Shelton A (2003) Cognitive maps and the hippocampus. Trends Cogn Neurosci 7(8):333–335

    Article  Google Scholar 

  • Niogi SN, Mukherjee P, Ghajar J, Johnson CE, Kolster R, Lee H, Sun M, Zimmerman R, Manley G, McCandliss B (2008) Structural dissociation of attentional control and memory in adults with and without mild traumatic brain injury. Brain 131:320–3221

    Article  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  CAS  PubMed  Google Scholar 

  • Pantano P, Mainero C, Caramia F (2006) Functional brain reorganization in multiple sclerosis: evidence from fMRI studies. J Neuroimage 16:104–114

    Article  Google Scholar 

  • Parslow D, Rose D, Brooks B, Fleminger S et al (2004) Allocentric spatial memory activation of the hippocampal formation measured with fMRI. Neuropsychology 18:450–461

    Article  PubMed  Google Scholar 

  • Perlstein WM, Cole MA, Demery JA, Seignourel PJ, Dixit NK, Larson MJ et al (2004) Parametric manipulation of working memory load in traumatic brain injury: behavioral and neural correlates. J Int Neuropsychol Soc 10(5):724–741

    Article  PubMed  Google Scholar 

  • Ptito A, Chen J-K, Johnston K (2007) Contribution of functional magnetic resonance imaging (fMRI) to sport concussion evaluation. Neurorehabilitation 22:217–227

    PubMed  Google Scholar 

  • Reddy CC, Collins MW (2009) Sports concussion: management and predictors of outcome. Curr Sports Med Rep 8(1):10–15

    PubMed  Google Scholar 

  • Rosenbaum R, Furey M, Horwitz B, Grady C (2008) Altered connectivity among emotion-related brain regions during short-term memory in Alzheimer’s disease. Neurobiol Aging 10:724–741

    Google Scholar 

  • Sanchez-Carrion R, Fernandez-Esprjo D, Junque C, Falcon C, Burgallo N, Roig T, Bernabeu M, Torsmos J, Vendrell P (2008) A longitudinal fMRI study of working memory in severe TBI patients with diffuse axonal injury. Neuroimage 43:421–429

    Article  PubMed  Google Scholar 

  • Schrader H, Mickrevičiene D, Gleizniene R, Jakstiene S, Surkiene D, Stovner L, Obelieniene D (2009) Magnetic resonance imaging after most common form of concussion. BMC Med Imag 9(11) (this article is available from: http://www.biomedcentral.com/1471-2342/9/11)

  • Shaw N (2002) The neurophysiology of concussion. Prog Neurobiol 67:281–344

    Article  CAS  PubMed  Google Scholar 

  • Slobounov S, Sebastianelli W, Cao C, Slobounov E, Newell K (2007) Differential rate of recovery in athletes after first versus and second concussion episodes. Neurosurgery 61(2):238–244

    Article  Google Scholar 

  • Slobounov S, Cao C, Sebastianelli W, Slobounov E, Newell K (2008) Residual deficits from concussion as revealed by virtual time-to-contact measures of postural stability. Clin Neurophysiol 119(2):281–289

    Article  PubMed  Google Scholar 

  • Slobounov S, Cao C, Sebastianelli W (2009) Differential effect of single versus recurrent mild traumatic brain injuries on wavelet entropy measures of EEG. Clin Neurophysiol 120(5):862–867

    Article  PubMed  Google Scholar 

  • Tollard E, Galanaud D, Perlbarg V, Sanchez-Pena P, Le Fur Y, Abdennour L, Cozzone P, Lehericy S, Chiras J, Puybasset L (2009) Experience of diffusion tensor imaging and 1H spectroscopy for outcome prediction in severe traumatic brain injury: preliminary results. Crit Care Med 37(4):1448–1455

    Article  PubMed  Google Scholar 

  • Trouillas P, Tkayanagi T, Hallett M, Currier D, Subramony S, Wessel K, Bryer A, Diener H, Massaquoi S, Gomez C et al (1997) International cooperative ataxia rating scale for pharmacological assessment of the cerebellar syndrome. J Neurol Sci 145:205–211

    Article  CAS  PubMed  Google Scholar 

  • Voermans N, Petersson K, Daudey L, Weber B, van Spaendonck K, Kremer H, Fernández (2004) Interaction between the human hippocampus and the caudae nucleus during route recognition. Neuron 43:427–435

    Article  CAS  PubMed  Google Scholar 

  • Ward N (2005) Plasticity and the functional reorganization of the human brain. Int J Psychophysiol 58:158–161

    Article  PubMed  Google Scholar 

  • Wirth W, Hartmann T, Boecking S, Vorderer P, Klimmt C, Schramm H et al (2007) A process model of the formation of spatial presence experience. Med Psychol 9:493–525

    Google Scholar 

  • Witmer BG, Singer MJ (1998) Measuring presence in virtual environments: a presence questionnaire. Presence Teleop Virtual Environ 7:225–240

    Article  Google Scholar 

  • Zhou Y, Dougherty J, Hubner K, Bai B, Cannon RK, Hutson R (2008) Abnormal connectivity in the posterior cingulate and hippocampus in early Alzheimer’s disease and mild cognitive impairment. Alzheimers Dement 4(4):265–270

    Article  PubMed  Google Scholar 

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Acknowledgments

This study was supported by NIH Grant RO1 NS056227-01A2 “Identification of Athletes at Risk for Traumatic Brain Injury” awarded to Dr. Slobounov, PI. We would like to thank Elena Slobounov for VR programming and Dr. Susan Lemieux for fMRI design development. All human studies have been approved by the The Pennsylvania State University IRB and all subjects gave their informed consent prior to their inclusion in the study.

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Authors and Affiliations

  1. Department of Kinesiology, The Pennsylvania State University, 19 Recreation Building, University Park, PA, 16802, USA

    Semyon M. Slobounov, K. Zhang & B. Johnson

  2. Department of Psychology, The Pennsylvania State University, 612 Moore Building, University Park, PA, 16802, USA

    W. Ray

  3. Chandlee Laboratory, Social, Life and Engineering Sciences Imaging Center, The Pennsylvania State University, University Park, PA, 16802, USA

    D. Pennell

  4. Center for Sport Medicine and Hershey Medical School, The Pennsylvania State University, University Park, USA

    Semyon M. Slobounov & W. Sebastianelli

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  1. Semyon M. Slobounov
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  2. K. Zhang
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  3. D. Pennell
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  4. W. Ray
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  5. B. Johnson
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  6. W. Sebastianelli
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Correspondence to Semyon M. Slobounov.

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Slobounov, S.M., Zhang, K., Pennell, D. et al. Functional abnormalities in normally appearing athletes following mild traumatic brain injury: a functional MRI study. Exp Brain Res 202, 341–354 (2010). https://doi.org/10.1007/s00221-009-2141-6

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  • DOI: https://doi.org/10.1007/s00221-009-2141-6

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