Experimental Brain Research

, Volume 202, Issue 2, pp 341–354 | Cite as

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

  • Semyon M. SlobounovEmail author
  • K. Zhang
  • D. Pennell
  • W. Ray
  • B. Johnson
  • W. Sebastianelli
Research Article


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.


Concussion fMRI Virtual reality Spatial memory Spatial navigation 



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.


  1. 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 20:51–58CrossRefPubMedGoogle Scholar
  2. 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 197–220CrossRefGoogle Scholar
  3. 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)Google Scholar
  4. Bryant R, Harvey A (1999) Postconcussive symptoms and posttraumatic stress disorder after mind traumatic brain injury. J Nerv Ment Dis 187:302–305CrossRefPubMedGoogle Scholar
  5. Burgess N, Maguire A, O’Keefe J (2002) The human hippocampus and spatial and episodic memory. Neuron 35:625–641CrossRefPubMedGoogle Scholar
  6. Cantu R (2006) Concussion classification: ongoing controversy. In: Slobounov S, Sebastianelli W (eds) Foundations of sport-related brain injuries. Springer, NY, pp 87–111CrossRefGoogle Scholar
  7. 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)Google Scholar
  8. Chen JK, Johnston KM, Frey S, Petrides M, Worsley K, Ptito A (2004) Functional abnormalities in symptomatic concussed athletes: an fMRI study. Neuroimage 22:68–82CrossRefPubMedGoogle Scholar
  9. 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 78:1231–1238CrossRefGoogle Scholar
  10. 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):33–54CrossRefPubMedGoogle Scholar
  11. Curtis C, D’Esposito M (2003) Persistent activity in the prefrontal cortex during working memory. Trends Cogn Sci 7:415–423CrossRefPubMedGoogle Scholar
  12. 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 3:1–10CrossRefGoogle Scholar
  13. 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 YorkGoogle Scholar
  14. 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 2:189–210CrossRefGoogle Scholar
  15. 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 123:2040–2054CrossRefGoogle Scholar
  16. Garnett MR, Corkill RG, Blamire AM et al (2001) Altered cellular metabolism following traumatic brain injury: a magnetic resonance spectroscopy study. J Neurotrauma 18:231–240CrossRefPubMedGoogle Scholar
  17. Guskiewicz K (2003) Assessment of postural stability following sport-related concussion. Curr Sport Med Rep 2(1):24–30Google Scholar
  18. 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 65–84CrossRefGoogle Scholar
  19. 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 37:877–888CrossRefPubMedGoogle Scholar
  20. Hayes S, Ryan L, Schnyer D, Nadel L (2004) An fMRI study of episodic memory: retrieval of object, spatial and temporal information. Behav Neurosci 118:885–896CrossRefPubMedGoogle Scholar
  21. Hillary FG (2008) Neuroimaging of working memory dysfunction and the dilemma with brain reorganization hypotheses. J Int Neuropsychol Soc 14(4):526–534CrossRefPubMedGoogle Scholar
  22. 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):965–978CrossRefPubMedGoogle Scholar
  23. Hillary FG, Genova HM, Chiaravalloti ND, DeLuca J (2006) Prefrontal modulation of working memory performance in brain injury and disease. Hum Brain Mapp 27:837–847CrossRefPubMedGoogle Scholar
  24. 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 25:890–899CrossRefPubMedGoogle Scholar
  25. Jancke L, Cheetham M, Baumgartner T (2009) Virtual reality on the role or prefrontal cortex in adults and children. Front Neurosci 3(1):52–59CrossRefPubMedGoogle Scholar
  26. 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 25:738–745PubMedGoogle Scholar
  27. Janzen G, Weststeijn C (2007) Neural representation of object location and route direction: an evernt-related fMRI study. Brain Res 1165:116–125CrossRefPubMedGoogle Scholar
  28. Kessels R, Pastma A, Wijnalda E, Haan E (2000a) Frontal-lobe involvement in spatial memory: evidence from PET, fMRI, and lesion studies. Neuropsych Rev 10:101–113CrossRefGoogle Scholar
  29. 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 10:295–303Google Scholar
  30. 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):1147–1154CrossRefPubMedGoogle Scholar
  31. 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 98:296–301CrossRefPubMedGoogle Scholar
  32. 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):359–360Google Scholar
  33. Maldjian JA, Laurienti PJ, Burdette JB, Kraft RA (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19:1233–1239Google Scholar
  34. 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 53:1300–1308PubMedGoogle Scholar
  35. 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):1004–1012CrossRefPubMedGoogle Scholar
  36. 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 23:1450–1467CrossRefPubMedGoogle Scholar
  37. 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 43:176–184CrossRefGoogle Scholar
  38. McNamara T, Shelton A (2003) Cognitive maps and the hippocampus. Trends Cogn Neurosci 7(8):333–335CrossRefGoogle Scholar
  39. 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 131:320–3221CrossRefGoogle Scholar
  40. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefPubMedGoogle Scholar
  41. Pantano P, Mainero C, Caramia F (2006) Functional brain reorganization in multiple sclerosis: evidence from fMRI studies. J Neuroimage 16:104–114CrossRefGoogle Scholar
  42. Parslow D, Rose D, Brooks B, Fleminger S et al (2004) Allocentric spatial memory activation of the hippocampal formation measured with fMRI. Neuropsychology 18:450–461CrossRefPubMedGoogle Scholar
  43. 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):724–741CrossRefPubMedGoogle Scholar
  44. Ptito A, Chen J-K, Johnston K (2007) Contribution of functional magnetic resonance imaging (fMRI) to sport concussion evaluation. Neurorehabilitation 22:217–227PubMedGoogle Scholar
  45. Reddy CC, Collins MW (2009) Sports concussion: management and predictors of outcome. Curr Sports Med Rep 8(1):10–15PubMedGoogle Scholar
  46. 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 10:724–741Google Scholar
  47. 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 43:421–429CrossRefPubMedGoogle Scholar
  48. 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:
  49. Shaw N (2002) The neurophysiology of concussion. Prog Neurobiol 67:281–344CrossRefPubMedGoogle Scholar
  50. 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):238–244CrossRefGoogle Scholar
  51. 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):281–289CrossRefPubMedGoogle Scholar
  52. 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):862–867CrossRefPubMedGoogle Scholar
  53. 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):1448–1455CrossRefPubMedGoogle Scholar
  54. 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 145:205–211CrossRefPubMedGoogle Scholar
  55. 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 43:427–435CrossRefPubMedGoogle Scholar
  56. Ward N (2005) Plasticity and the functional reorganization of the human brain. Int J Psychophysiol 58:158–161CrossRefPubMedGoogle Scholar
  57. 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 9:493–525Google Scholar
  58. Witmer BG, Singer MJ (1998) Measuring presence in virtual environments: a presence questionnaire. Presence Teleop Virtual Environ 7:225–240CrossRefGoogle Scholar
  59. 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):265–270CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Semyon M. Slobounov
    • 1
    • 4
    Email author
  • K. Zhang
    • 1
  • D. Pennell
    • 3
  • W. Ray
    • 2
  • B. Johnson
    • 1
  • W. Sebastianelli
    • 4
  1. 1.Department of KinesiologyThe Pennsylvania State UniversityUniversity ParkUSA
  2. 2.Department of PsychologyThe Pennsylvania State UniversityUniversity ParkUSA
  3. 3.Chandlee Laboratory, Social, Life and Engineering Sciences Imaging CenterThe Pennsylvania State UniversityUniversity ParkUSA
  4. 4.Center for Sport Medicine and Hershey Medical SchoolThe Pennsylvania State UniversityUniversity ParkUSA

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