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Acute and Subacute Changes in Neural Activation during the Recovery from Sport-Related Concussion

Published online by Cambridge University Press:  08 July 2013

Thomas A. Hammeke ,
Michael McCrea ,
Sarah M. Coats ,
Matthew D. Verber ,
Sally Durgerian ,
Kristin Flora ,
Gary S. Olsen ,
Peter D. Leo ,
Thomas A. Gennarelli  and
Stephen M. Rao
Thomas A. Hammeke*
Affiliation:
Clement J. Zablocki VA Medical Center & Department of Psychiatry & Behavioral Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin
Michael McCrea
Affiliation:
Department of Neurosurgery, Medical College of Wisconsin, Milwaukee, Wisconsin
Sarah M. Coats
Affiliation:
Rehabilitation Institute at St. Mary's Hospital, Enid, Oklahoma
Matthew D. Verber
Affiliation:
Department of Chemistry, University of North Carolina, Chapel Hill, North Carolina
Sally Durgerian
Affiliation:
Department of Neurology, Medical College of Wisconsin, Milwaukee, Wisconsin
Kristin Flora
Affiliation:
Department of Psychology, Franklin College, Franklin, Indiana
Gary S. Olsen
Affiliation:
Department of Neuropsychology, Marshfield Clinic, Marshfield, Wisconsin
Peter D. Leo
Affiliation:
Department of Neurology, Medical College of Wisconsin, Milwaukee, Wisconsin
Thomas A. Gennarelli
Affiliation:
Department of Neurosurgery, Medical College of Wisconsin, Milwaukee, Wisconsin
Stephen M. Rao
Affiliation:
Schey Center for Cognitive Neuroimaging, Neurological Institute, Cleveland Clinic, Cleveland, Ohio
*
Correspondence and reprint requests to: Thomas A. Hammeke, Clement J. Zablocki VA Medical Center, Acute Mental Health—Neuropsychology, Bldg 111, Room 3301, 5000 W. National Avenue, Milwaukee, WI 53295. E-mail: [email protected]
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Abstract

To study the natural recovery from sports concussion, 12 concussed high school football athletes and 12 matched uninjured teammates were evaluated with symptom rating scales, tests of postural balance and cognition, and an event-related fMRI study during performance of a load-dependent working memory task at 13 h and 7 weeks following injury. Injured athletes showed the expected postconcussive symptoms and cognitive decline with decreased reaction time (RT) and increased RT variability on a working memory task during the acute period and an apparent full recovery 7 weeks later. Brain activation patterns showed decreased activation of right hemisphere attentional networks in injured athletes relative to controls during the acute period with a reversed pattern of activation (injured > controls) in the same networks at 7 weeks following injury. These changes coincided with a decrease in self-reported postconcussive symptoms and improved cognitive test performance in the injured athletes. Results from this exploratory study suggest that decreased activation of right hemisphere attentional networks mediate the cognitive changes and postconcussion symptoms observed during the acute period following concussion. Conversely, improvement in cognitive functioning and postconcussive symptoms during the subacute period may be mediated by compensatory increases in activation of this same attentional network. (JINS, 2013, 19, 1–10)

Keywords

fMRIBrain activationMild TBICognitive compensationBrain injuryAttention networks
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 19 , Issue 8 , September 2013 , pp. 863 - 872
Copyright
Copyright © The International Neuropsychological Society 2013 

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References

Arrington, C.M., Carr, T.H., Mayer, A.R., Rao, S.M. (2000). Neural mechanisms of visual attention: Object-based selection of a region in space. Journal of Cognitive Neuroscience, 12, 106–117.CrossRefGoogle ScholarPubMed
Belanger, H.G., Vanderploeg, R.D. (2005). The neuropsychological impact of sport-related concussion: A meta-analysis. Journal of International Neuropsychological Society, 11, 345–357.CrossRefGoogle Scholar
Broglio, S.P., Puetz, T.W. (2008). The effect of sport concussion on neurocognitive function, self-report symptoms and postural control: A meta-analysis. Sports Medicine, 38, 53–67.CrossRefGoogle ScholarPubMed
Chen, J.-K., Johnston, K.M., Frey, S., Petrides, M., Worsley, K., Ptito, A. (2004). Functional abnormalities in symptomatic concussed athletes: An fMRI study. Neuroimage, 22, 68–82.CrossRefGoogle ScholarPubMed
Chen, J.-K., Johnston, K.M., Petrides, M., Ptito, A. (2008a). Neural substrates of symptoms of depression following concussion in male athletes with persisting postconcussion symptoms. Archive of General Psychiatry, 65, 81–89.CrossRefGoogle ScholarPubMed
Chen, J.-K., Johnston, K.M., Petrides, M., Ptito, A. (2008b). Recovery from mild head injury in sports: Evidence from serial functional magnetic resonance imaging studies in male athletes. Clinical Journal of Sports Medicine, 18, 241–247.CrossRefGoogle ScholarPubMed
Chen, S.H.A., Kareken, D.A., Fastenau, P.S., Trexler, L.E., Hutchins, G.D. (2003). A study of persistent post-concussion symptoms in mild head trauma using positron emission tomography. Journal of Neurology, Neurosurgery, & Psychiatry, 74, 326–332.CrossRefGoogle ScholarPubMed
Collins, M.W., Grindel, S.H., Lovell, M.R., Dede, D.E., Moser, D.J., Phalin, B.R., McKeag, D.B. (1999). Relationship between concussion and neuropsychological performance in college football players. Journal of American Medical Association, 282, 964–970.CrossRefGoogle ScholarPubMed
Corbetta, M., Shulman, G.L. (2011). Spatial neglect and attention networks. Annual Review of Neuroscience, 34, 569–599.CrossRefGoogle ScholarPubMed
Guskiewicz, K.M., McCrea, M., Marshall, S.W., Cantu, R.C., Randolph, C., Barr, W., Kelly, J.P. (2003). Cumulative effects associated with recurrent concussion in collegiate football players: The NCAA Concussion Study. Journal of American Medical Association, 290, 2549–2555.CrossRefGoogle ScholarPubMed
Halterman, C.I., Langan, J., Drew, A., Rodriguez, E., Osternig, L.R., Chou, L.-S., van Donkelaar, P.l. (2006). Tracking the recovery of visuospatial attention deficits in mild traumatic brain injury. Brain, 129, 747–753.CrossRefGoogle ScholarPubMed
Heilman, K.M., Watson, R.T., Valenstein, E. (2012). Neglect and related disorders. In K. M. Heilman & E. E. Valenstein's (Eds.), Clinical neuropsychology (5th ed.). New York: Oxford University Press.Google Scholar
Jantzen, K.J., Anderson, B., Steinberg, F.L., Kelso, J.A. (2004). A prospective functional MR imaging study of mild traumatic brain injury in college football players. AJNR American Journal of Neuroradiology, 25, 738–745.Google ScholarPubMed
Johnson, B., Zhang, K., Gay, M., Horovitz, S., Hallett, M., Sebastianelli, W., Slobounov, S. (2012). Alteration of brain default network in subacute phase of injury in concussed individuals: Resting-state fMRI study. Neuroimage, 59, 511–518.CrossRefGoogle ScholarPubMed
Kumar, S., Rao, S.L., Chandramouli, B.A., Pillai, S.V. (2009). Reduction of functional brain connectivity in mild traumatic brain injury during working memory. Journal of Neurotrauma, 26, 665–675.CrossRefGoogle ScholarPubMed
Lovell, M.R., Collins, M.W. (1998). Neuropsychological assessment of the college football player. Journal of Head Trauma Rehabilitation, 13, 9–26.CrossRefGoogle ScholarPubMed
Lovell, M.R., Pardini, J.E., Welling, J., Collins, M.W., Bakal, J., Lazar, N., Becker, J.T. (2007). Functional brain abnormalities are related to recovery and time return-to-play in athletes. Neurosurgery, 61, 352–359.CrossRefGoogle ScholarPubMed
Macciocchi, S.N., Barth, J.T., Alves, W., Rimel, R.W., Jane, J.A. (1996). Neuropsychological functioning and recovery after mild head injury in collegiate athletes. Neurosurgery, 39, 510–514.CrossRefGoogle ScholarPubMed
Malojcic, B., Mubrin, Z., Coric, B., Susnic, M., Spilich, G.J. (2008). Consequences of mild traumatic brain injury on information processing assessed with attention and short-term memory tasks. Journal of Neurotrauma, 25, 30–37.CrossRefGoogle ScholarPubMed
Mayer, A.R., Mannell, M.V., Ling, J., Elgie, R., Gasparovic, C., Phillips, J.P., Yeo, R.A. (2009). Auditory orienting and inhibition of return in mild traumatic brain injury: A fMRI study. Human Brain Mapping, 30, 4152–4166.CrossRefGoogle ScholarPubMed
McCrea, M. (2001). Standardized mental status testing on the sideline after sport-related concussion. Journal of Athletic Training, 36, 274–279.Google ScholarPubMed
McCrea, M., Guskiewicz, K.M., Marshall, S.W., Barr, W., Randolph, C., Cantu, R.C., Kelly, J.P. (2003). Acute effects and recovery time following concussion in collegiate football players: The NCAA Concussion Study. Journal of American Medical Association, 290, 2556–2563.CrossRefGoogle ScholarPubMed
McCrea, M., Hammeke, T.A., Olsen, G., Leo, P., Guskiewicz, K. (2004). Unreported concussion in high school football players: Implications for prevention. Clinical Journal of Sports Medicine, 14, 13–17.CrossRefGoogle ScholarPubMed
Mesulam, M. (2000). Attentional networks, confusional states and neglect syndromes. In M. Mesulam (Ed.), Principles of behavioral and cognitive neurology. New York: Oxford University Press.CrossRefGoogle Scholar
Narayanan, N.S., Prabhakaran, V., Bunge, S.A., Christoff, K., Fine, E.M., Gabrieli, J.D. (2005). The role of the prefrontal cortex in the maintenance of verbal working memory: An event-related fMRI analysis. Neuropsychology, 19(2), 223–232.CrossRefGoogle ScholarPubMed
Newsome, M.R., Steinberg, J.L., Scheibel, R.S., Troyanskaya, M., Chu, Z., Hanten, G., Levin, H.S. (2008). Effects of traumatic brain injury on working memory-related brain activation in adolescents. Neuropsychology, 22, 419–425.CrossRefGoogle ScholarPubMed
Pardini, J.E., Pardini, D.A., Becker, J.T., Dunfee, K.L., Eddy, W.F., Lovell, M.R., Welling, J.S. (2010). Postconcussive symptoms are associated with compensatory cortical recruitment during a working memory task. Neurosurgery, 67, 1020–1027.CrossRefGoogle ScholarPubMed
Practice Parameter: The management of concussion in sports (summary statement). Report of the Quality Standards Subcommittee. (1997). Neurology, 48, 581–585.CrossRefGoogle Scholar
Sadek, J.R., Hammeke, T.A. (2002). Functional neuroimaging in neurology and psychiatry. CNS Spectrums, 7, 286–299.CrossRefGoogle ScholarPubMed
Slobounov, S.M., Zhang, K., Pennell, D., Ray, W., Johnson, B., Sebastianelli, W. (2010). Functional abnormalities in normally appearing athletes following mild traumatic brain injury: A functional MRI study. Experimental Brain Research, 202, 341–354.CrossRefGoogle ScholarPubMed
Sternberg, S. (1966). High-speed scanning in human memory. Science, 153, 652–654.CrossRefGoogle ScholarPubMed