Skip to main content
Log in

A resting state functional magnetic resonance imaging study of concussion in collegiate athletes

Brain Imaging and Behavior Aims and scope Submit manuscript

An Erratum to this article was published on 18 October 2014

Abstract

Sports-related concussions are currently diagnosed through multi-domain assessment by a medical professional and may utilize neurocognitive testing as an aid. However, these tests have only been able to detect differences in the days to week post-concussion. Here, we investigate a measure of brain function, namely resting state functional connectivity, which may detect residual brain differences in the weeks to months after concussion. Twenty-one student athletes (9 concussed within 6 months of enrollment; 12 non-concussed; between ages 18 and 22 years) were recruited for this study. All participants completed the Wisconsin Card Sorting Task and the Color-Word Interference Test. Neuroimaging data, specifically resting state functional Magnetic Resonance Imaging data, were acquired to examine resting state functional connectivity. Two sample t-tests were used to compare the neurocognitive scores and resting state functional connectivity patterns among concussed and non-concussed participants. Correlations between neurocognitive scores and resting state functional connectivity measures were also determined across all subjects. There were no significant differences in neurocognitive performance between concussed and non-concussed groups. Concussed subjects had significantly increased connections between areas of the brain that underlie executive function. Across all subjects, better neurocognitive performance corresponded to stronger brain connectivity. Even at rest, brains of concussed athletes may have to ‘work harder’ than their healthy peers to achieve similar neurocognitive results. Resting state brain connectivity may be able to detect prolonged brain differences in concussed athletes in a more quantitative manner than neurocognitive test scores.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Allen, E. A., Erhardt, E. B., Damaraju, E., Gruner, W., Segall, J. M., Silva, R. F., et al. (2011). A baseline for the multivariate comparison of resting-state networks. Frontiers in Systems Neuroscience, 5.

  • Belanger, H. G., & Vanderploeg, R. D. (2005). The neuropsychological impact of sports-related concussion: a meta-analysis. Journal of the International Neuropsychological Society, 11(4), 345–357.

    Article  PubMed  Google Scholar 

  • Berg, E. A. (1948). A simple objective technique for measuring flexibility in thinking. The Journal of General Psychology, 39(1), 15–22.

    Article  CAS  PubMed  Google Scholar 

  • Blakemore, S. (2008). The social brain in adolescence. Nature Reviews. Neuroscience, 9(4), 267–277.

    Article  CAS  PubMed  Google Scholar 

  • Blennow, K., Hardy, J., & Zetterberg, H. (2012). The neuropathology and neurobiology of traumatic brain injury. Neuron, 76(5), 886–899.

    Article  CAS  PubMed  Google Scholar 

  • Broglio, S. P., & Puetz, T. W. (2008). The effect of sport concussion on neurocognitive function, self-report symptoms and postural control. Sports Medicine, 38(1), 53–67.

    Article  PubMed  Google Scholar 

  • Buchsbaum, B. R., Greer, S., Chang, W., & Berman, K. F. (2005). Meta‐analysis of neuroimaging studies of the Wisconsin card‐sorting task and component processes. Human Brain Mapping, 25(1), 35–45.

    Article  PubMed  Google Scholar 

  • Buckner, R. L., Andrews‐Hanna, J. R., & Schacter, D. L. (2008). The brain’s default network. Annals of the New York Academy of Sciences, 1124(1), 1–38.

    Article  PubMed  Google Scholar 

  • Chai, X. J., Whitfield-Gabrieli, S., Shinn, A. K., Gabrieli, J. D., Castañón, A. N., McCarthy, J. M., et al. (2011). Abnormal medial prefrontal cortex resting-state connectivity in bipolar disorder and schizophrenia. Neuropsychopharmacology, 36(10), 2009–2017.

    Article  PubMed Central  PubMed  Google Scholar 

  • Conklin, S. M., Gianaros, P. J., Brown, S. M., Yao, J. K., Hariri, A. R., Manuck, S. B., & Muldoon, M. F. (2007). Long-chain omega-3 fatty acid intake is associated positively with corticolimbic gray matter volume in healthy adults. Neuroscience Letters, 421(3), 209–212.

    Article  CAS  PubMed  Google Scholar 

  • Cullen, K. R., Gee, D. G., Klimes-Dougan, B., Gabbay, V., Hulvershorn, L., Mueller, B. A., et al. (2009). A preliminary study of functional connectivity in comorbid adolescent depression. Neuroscience Letters, 460(3), 227–231.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Damoiseaux, J., Rombouts, S., Barkhof, F., Scheltens, P., Stam, C., Smith, S. M., & Beckmann, C. (2006). Consistent resting-state networks across healthy subjects. Proceedings of the National Academy of Sciences, 103(37), 13848–13853.

    Article  CAS  Google Scholar 

  • Damoiseaux, J. S., Beckmann, C. F., Arigita, E. J., Barkhof, F., Scheltens, P., Stam, C. J., et al. (2008). Reduced resting-state brain activity in the “default network” in normal aging. Cerebral Cortex (New York, N.Y.: 1991), 18(8), 1856–1864.

  • Delis, D. C., Kaplan, E., & Kramer, J. H. (2001). Delis-kaplan executive function system (D-KEFS) Psychological Corporation.

  • Duhaime, A., Beckwith, J. G., Maerlender, A. C., McAllister, T. W., Crisco, J. J., Duma, S. M., et al. (2012). Spectrum of acute clinical characteristics of diagnosed concussions in college athletes wearing instrumented helmets: clinical article. Journal of Neurosurgery, 117(6), 1092–1099.

    Article  PubMed Central  PubMed  Google Scholar 

  • Echemendia, R. J., Putukian, M., Mackin, R. S., Julian, L., & Shoss, N. (2001). Neuropsychological test performance prior to and following sports-related mild traumatic brain injury. Clinical Journal of Sport Medicine, 11(1), 23–31.

    Article  CAS  PubMed  Google Scholar 

  • Friston, K. J. (1994). Functional and effective connectivity in neuroimaging: a synthesis. Human Brain Mapping, 2, 56–78.

  • Gardner, A., Kay-Lambkin, F., Stanwell, P., Donnelly, J., Williams, W. H., Hiles, A., et al. (2012). A systematic review of diffusion tensor imaging findings in sports-related concussion. Journal of Neurotrauma, 29(16), 2521–2538.

    Article  PubMed  Google Scholar 

  • Grindel, S. H., Lovell, M. R., & Collins, M. W. (2001). The assessment of sport-related concussion: the evidence behind neuropsychological testing and management. Clinical Journal of Sport Medicine, 11(3), 134–143.

    Article  CAS  PubMed  Google Scholar 

  • Hayama, H. R., & Rugg, M. D. (2009). Right dorsolateral prefrontal cortex is engaged during post-retrieval processing of both episodic and semantic information. Neuropsychologia, 47(12), 2409–2416.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hebb, D. (1949). The organization of behavior: a neuropsychological theory.

  • Hunt, T. N., Ferrara, M. S., Miller, L. S., & Macciocchi, S. (2007). The effect of effort on baseline neuropsychological test scores in high school football athletes. Archives of Clinical Neuropsychology, 22(5), 615–621.

    Article  PubMed  Google Scholar 

  • 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(1), 511–518.

    Article  PubMed Central  PubMed  Google Scholar 

  • Kelly, A. C., Di Martino, A., Uddin, L. Q., Shehzad, Z., Gee, D. G., Reiss, P. T., et al. (2009). Development of anterior cingulate functional connectivity from late childhood to early adulthood. Cerebral Cortex, 19(3), 640–657.

    Article  PubMed  Google Scholar 

  • Laird, A. R., McMillan, K. M., Lancaster, J. L., Kochunov, P., Turkeltaub, P. E., Pardo, J. V., & Fox, P. T. (2005). A comparison of label‐based review and ALE meta‐analysis in the stroop task. Human Brain Mapping, 25(1), 6–21.

    Article  PubMed  Google Scholar 

  • Langlois, J. A., Rutland-Brown, W., & Wald, M. M. (2006). The epidemiology and impact of traumatic brain injury: a brief overview. The Journal of Head Trauma Rehabilitation, 21(5), 375–378.

    Article  PubMed  Google Scholar 

  • Leung, H., Skudlarski, P., Gatenby, J. C., Peterson, B. S., & Gore, J. C. (2000). An event-related functional MRI study of the stroop color word interference task. Cerebral Cortex, 10(6), 552–560.

    Article  CAS  PubMed  Google Scholar 

  • Lie, C., Specht, K., Marshall, J. C., & Fink, G. R. (2006). Using fMRI to decompose the neural processes underlying the wisconsin card sorting test. NeuroImage, 30(3), 1038–1049.

    Article  PubMed  Google Scholar 

  • MacDonald, A. W., Cohen, J. D., Stenger, V. A., & Carter, C. S. (2000). Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science, 288(5472), 1835–1838.

    Article  CAS  PubMed  Google Scholar 

  • Mahaffey, B. L. (2012). Concussions in high school sports: are they worth the risk? should school football be banned? Missouri Medicine, 109(6), 445–449.

    PubMed  Google Scholar 

  • Margulies, D. S., Kelly, A., Uddin, L. Q., Biswal, B. B., Castellanos, F. X., & Milham, M. P. (2007). Mapping the functional connectivity of anterior cingulate cortex. NeuroImage, 37(2), 579–588.

    Article  PubMed  Google Scholar 

  • Marquez de la Plata, Carlos, D., Garces, J., Shokri Kojori, E., Grinnan, J., Krishnan, K., Pidikiti, R., et al. (2011). Deficits in functional connectivity of hippocampal and frontal lobe circuits after traumatic axonal injury. Archives of Neurology, 68(1), 74.

    Article  PubMed Central  PubMed  Google Scholar 

  • Mayer, A. R., Mannell, M. V., Ling, J., Gasparovic, C., & Yeo, R. A. (2011). Functional connectivity in mild traumatic brain injury. Human Brain Mapping, 32(11), 1825–1835.

    Article  PubMed Central  PubMed  Google Scholar 

  • McCrory, P., Meeuwisse, W. H., Aubry, M., Cantu, B., Dvořák, J., Echemendia, R. J., et al. (2013). Consensus statement on concussion in sport: the 4th international conference on concussion in sport held in zurich, november 2012. British Journal of Sports Medicine, 47(5), 250–258.

    Article  PubMed  Google Scholar 

  • Monchi, O., Petrides, M., Petre, V., Worsley, K., & Dagher, A. (2001). Wisconsin card sorting revisited: distinct neural circuits participating in different stages of the task identified by event-related functional magnetic resonance imaging. The Journal of Neuroscience, 21(19), 7733–7741.

    CAS  PubMed  Google Scholar 

  • Qin, S., Hermans, E. J., van Marle, H. J., Luo, J., & Fernández, G. (2009). Acute psychological stress reduces working memory-related activity in the dorsolateral prefrontal cortex. Biological Psychiatry, 66(1), 25–32.

    Article  PubMed  Google Scholar 

  • Raichle, M. E., & Snyder, A. Z. (2007). A default mode of brain function: a brief history of an evolving idea. NeuroImage, 37(4), 1083–1090.

    Article  PubMed  Google Scholar 

  • Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., & Shulman, G. L. (2001). A default mode of brain function. Proceedings of the National Academy of Sciences of the United States of America, 98(2), 676–682. doi:10.1073/pnas.98.2.676.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schatz, P., & Sandel, N. (2013). Sensitivity and specificity of the online version of ImPACT in high school and collegiate athletes. The American Journal of Sports Medicine, 41(2), 321–326.

    Article  PubMed  Google Scholar 

  • Seeley, W. W., Menon, V., Schatzberg, A. F., Keller, J., Glover, G. H., Kenna, H., et al. (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. The Journal of Neuroscience, 27(9), 2349–2356.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sharp, D. J., Beckmann, C. F., Greenwood, R., Kinnunen, K. M., Bonnelle, V., De Boissezon, X., et al. (2011). Default mode network functional and structural connectivity after traumatic brain injury. Brain, 134(8), 2233–2247.

    Article  PubMed  Google Scholar 

  • Silton, R. L., Heller, W., Towers, D. N., Engels, A. S., Spielberg, J. M., Edgar, J. C., et al. (2010). The time course of activity in dorsolateral prefrontal cortex and anterior cingulate cortex during top-down attentional control. NeuroImage, 50(3), 1292–1302.

    Article  PubMed  Google Scholar 

  • Slobounov, S., Gay, M., Zhang, K., Johnson, B., Pennell, D., Sebastianelli, W., et al. (2011). Alteration of brain functional network at rest and in response to YMCA physical stress test in concussed athletes: RsFMRI study. NeuroImage, 55(4), 1716–1727.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Song, X. W., Dong, Z. Y., Long, X. Y., Li, S. F., Zuo, X. N., Zhu, C. Z., et al. (2011). REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PloS One, 6(9), e25031. doi:10.1371/journal.pone.0025031.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Staudinger, M. R., Erk, S., & Walter, H. (2011). Dorsolateral prefrontal cortex modulates striatal reward encoding during reappraisal of reward anticipation. Cerebral Cortex, 21(11), 2578–2588.

    Article  PubMed  Google Scholar 

  • Stroop, J. R. (1935). Studies of interference in serial verbal reactions. Journal of Experimental Psychology, 18(6), 643.

    Article  Google Scholar 

  • Tsushima, W. T., Shirakawa, N., & Geling, O. (2013). Neurocognitive functioning and symptom reporting of high school athletes following a single concussion. Applied Neuropsychology: Child, 2(1), 13–16.

    Article  Google Scholar 

Download references

Acknowledgments

The authors would like to thank the Department of Radiology and the Advanced MR Imaging Core at the University of Massachusetts Medical School. The project described was supported by an award from the Department of Radiology, University of Massachusetts Medical School (UMMS). MRI studies were conducted at the Advanced MR Imaging Center, UMMS, with support from Shaokuan Zheng, PhD. The authors would also like to thank the athletic trainers at Clark University and the College of the Holy Cross for their recruitment efforts.

Funding source

National Institute of Mental Health to CMM (MH073998), and start-up funds to CMM from the University of Massachusetts Medical School. Swiss National Science Foundation (PBGEP3-134252) to AAL.

Conflict of interest

Suzanne Czerniak, Elif Sikoglu, Ana Liso Navarro, Joseph McCafferty, Jordan Eisenstock, J Herbert Stevenson, Jean King, and Constance Moore declare that they have no conflict of interest.

Informed consent statement

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, as revised in 2000 . Informed consent was obtained from all patients for being included in the study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Constance M. Moore.

Additional information

Suzanne M Czerniak and Elif M Sikoglu contributed equally to this work

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Czerniak, S.M., Sikoglu, E.M., Liso Navarro, A.A. et al. A resting state functional magnetic resonance imaging study of concussion in collegiate athletes. Brain Imaging and Behavior 9, 323–332 (2015). https://doi.org/10.1007/s11682-014-9312-1

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-014-9312-1

Keywords

Navigation