Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Are there any differential responses to concussive injury in civilian versus athletic populations: a neuroimaging study

  • 201 Accesses


Accurate identification and classification of patients suffering from mild traumatic brain injury (mTBI) is a significant challenge faced by clinicians and researchers. To examine if there are different pathophysiological responses to concussive injury in different populations, evaluated here comparing collegiate athletes versus age-matched non-athletes. Resting-state fMRI data were acquired in the acute phase of concussion from 30 collegiate athletes and from 30 injury and age matched non-athletes. Resting-state functional connectivity measures revealed group differences with reduced connectivity in the anterior cingulate cortex (p < .05) and posterior cingulate cortex (p < 0.05) hubs of the Default Mode Network in the athletes. Given the known positive effects of exercise on brain functional reserves and neural efficiency concept, we expected less pronounced effect of concussion in athletic population. In contrast, there were significant decreases in functional connectivity in athletes that could be a result of previous repetitive subconcussive impacts and history of concussion.

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

Fig. 1
Fig. 2

Change history

  • 19 November 2018

    The original version of this article contained mistakes in the article title, and the authors would like to correct them. The article title should be “Are there any differential responses to concussive injury in civilian versus athletic populations: a neuroimaging study”.


  1. Ahlskog, J. E. (2011). Does vigorous exercise have a neuroprotective effect in Parkinson disease? Neurology, 77(3), 288–294.

  2. Amorini, A. M., Lazzarino, G., Di Pietro, V., Signoretti, S., Lazzarino, G., Belli, A., & Tavazzi, B. (2017). Severity of experimental traumatic brain injury modulates changes in concentrations of cerebral free amino acids. Journal of Cellular and Molecular Medicine, 21(3), 530–542.

  3. Anderson, T., Heitger, M., & Macleod, A. (2006). Concussion and mild head injury. Practical Neurology, 6(6), 342–357.

  4. Baugh, C. M., Stamm, J. M., Riley, D. O., Gavett, B. E., Shenton, M. E., Lin, A., Nowinski, C. J., Cantu, R. C., McKee, A. C., & Stern, R. A. (2012). Chronic traumatic encephalopathy: Neurodegeneration following repetitive concussive and subconcussive brain trauma. Brain Imaging and Behavior, 6(2), 244–254. https://doi.org/10.1007/s11682-012-9164-5.

  5. Bergman, K., & Bay, E. (2010). Mild traumatic brain injury/concussion: A review for ED nurses. Journal of Emergency Nursing, 36(3), 221–230. https://doi.org/10.1016/j.jen.2009.07.001.

  6. Bosnell, R., Wegner, C., Kincses, Z. T., Korteweg, T., Agosta, F., Ciccarelli, O., et al. (2008). Reproducibility of fMRI in the clinical setting: Implications for trial designs. Neuroimage, 42(2), 603–610.

  7. Brier, M. R., Thomas, J. B., & Ances, B. M. (2014). Network dysfunction in Alzheimer's disease: Refining the disconnection hypothesis. Brain Connectivity, 4(5), 299–311.

  8. Büchel, C., & Friston, K. (1997). Modulation of connectivity in visual pathways by attention: Cortical interactions evaluated with structural equation modelling and fMRI. Cerebral Cortex, 7(8), 768–778.

  9. Cantu, R. (2006). Concussion Classification: Ongoing Controversy. In S. Slobounov & W. Sebastianelli (Eds.), Foundations of Sport-Related Brain Injuries (pp. 87–110). US: Springer.

  10. Cantu, R. C. (2007). Athletic concussion current understanding as of 2007. Neurosurgery, 60(6), 963–964. https://doi.org/10.1227/01.neu.0000255430.62291.7b.

  11. Chaddock, L., Erickson, K. I., Prakash, R. S., Kim, J. S., Voss, M. W., VanPatter, M., . . . Kramer, A. F. (2010). A neuroimaging investigation of the association between aerobic fitness, hippocampal volume, and memory performance in preadolescent children. Brain Research, 1358, 172–183. doi:https://doi.org/10.1016/j.brainres.2010.08.049.

  12. Costafreda, S. G. (2009). Pooling fMRI data: Meta-analysis, mega-analysis and multi-center studies. Frontiers in Neuroinformatics, 3, 33.

  13. Coynel, D., Marrelec, G., Perlbarg, V., Pélégrini-Issac, M., Van de Moortele, P.-F., Ugurbil, K., . . . Lehéricy, S. (2010). Dynamics of motor-related functional integration during motor sequence learning. Neuroimage, 49(1), 759–766.

  14. Di Pietro, V., Lazzarino, G., Amorini, A. M., Signoretti, S., Hill, L. J., Porto, E., et al. (2017). Fusion or fission: The Destiny of mitochondria in traumatic brain injury of different severities. Scientific Reports, 7(1), 9189.

  15. Doppenberg, E. M., Choi, S. C., & Bullock, R. (2004). Clinical trials in traumatic brain injury: Lessons for the future. Journal of Neurosurgical Anesthesiology, 16(1), 87–94.

  16. Fischer, B. L., Parsons, M., Durgerian, S., Reece, C., Mourany, L., Lowe, M. J., et al. (2014). Neural activation during response inhibition differentiates blast from mechanical causes of mild to moderate traumatic brain injury. Journal of Neurotrauma, 31(2), 169–179.

  17. Fletcher, P., Büchel, C., Josephs, O., Friston, K., & Dolan, R. (1999). Learning-related neuronal responses in prefrontal cortex studied with functional neuroimaging. Cerebral Cortex, 9(2), 168–178.

  18. Forman, S. D., Cohen, J. D., Fitzgerald, M., Eddy, W. F., Mintun, M. A., & Noll, D. C. (1995). Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): Use of a cluster-size threshold. Magnetic Resonance in Medicine, 33(5), 636–647.

  19. Fox, M. D., & Raichle, M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nature Reviews Neuroscience, 8(9), 700–711.

  20. Franco, A. R., Pritchard, A., Calhoun, V. D., & Mayer, A. R. (2009). Interrater and intermethod reliability of default mode network selection. Human Brain Mapping, 30(7), 2293–2303.

  21. Gountouna, V.-E., Job, D. E., McIntosh, A. M., Moorhead, T. W. J., Lymer, G. K. L., Whalley, H. C., et al. (2010). Functional magnetic resonance imaging (fMRI) reproducibility and variance components across visits and scanning sites with a finger tapping task. Neuroimage, 49(1), 552–560.

  22. Gradin, V., Gountouna, V.-E., Waiter, G., Ahearn, T. S., Brennan, D., Condon, B., et al. (2010). Between-and within-scanner variability in the CaliBrain study n-back cognitive task. Psychiatry Research: Neuroimaging, 184(2), 86–95.

  23. Guskiewicz, K. M., McCrea, M., Marshall, S. W., Cantu, R. C., Randolph, C., Barr, W., et al. (2003). Cumulative effects associated with recurrent concussion in collegiate football players: The NCAA concussion study. Jama, 290(19), 2549–2555.

  24. Johnson, B., Gay, M., Zhang, K., Neuberger, T., Horovitz, S. G., Hallett, M., et al. (2012a). The use of magnetic resonance spectroscopy in the subacute evaluation of athletes recovering from single and multiple mild traumatic brain injury. Journal of Neurotrauma, 29(13), 2297–2304. https://doi.org/10.1089/neu.2011.2294.

  25. Johnson, B., Zhang, K., Gay, M., Horovitz, S., Hallett, M., Sebastianelli, W., & Slobounov, S. (2012b). Alteration of brain default network in subacute phase of injury in concussed individuals: Resting-state fMRI study. Neuroimage, 59(1), 511–518. https://doi.org/10.1016/j.neuroimage.2011.07.081.

  26. Johnson, B. D., Neuberger, T., Gay, M., Hallett, M., & Slobounov, S. (2014). Effects of subconcussive head trauma on the default mode network of the brain. Journal of Neurotrauma, 31, 1907–1913. https://doi.org/10.1089/neu.2014.3415.

  27. Kiraly, M. A., & Kiraly, S. J. (2007). Traumatic brain injury and delayed sequelae: A review-traumatic brain injury and mild traumatic brain injury (concussion) are precursors to later-onset brain disorders, including early-onset dementia. The Scientific World Journal, 7, 1768–1776.

  28. Krajcovicova, L., Mikl, M., Marecek, R., & Rektorova, I. (2012). The default mode network integrity in patients with Parkinson’s disease is levodopa equivalent dose-dependent. Journal of Neural Transmission, 119(4), 443–454.

  29. Langlois, J. A., Rutland-Brown, W., & Thomas, K. E. (2005). The incidence of traumatic brain injury among children in the United States - differences by race. Journal of Head Trauma Rehabilitation, 20(3), 229–238.

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

  31. Ma, L., Narayana, S., Robin, D. A., Fox, P. T., & Xiong, J. (2011). Changes occur in resting state network of motor system during 4weeks of motor skill learning. Neuroimage, 58(1), 226–233.

  32. Machulda, M. M., Jones, D. T., Vemuri, P., McDade, E., Avula, R., Przybelski, S., . . . Jack, C. R. (2011). Effect of APOE ε4 status on intrinsic network connectivity in cognitively normal elderly subjects. Archives of Neurology, 68(9), 1131–1136.

  33. Marshall, L. F. (2000). Head injury: Recent past, present, and future. Neurosurgery, 47(3), 546–561.

  34. Mayer, A. R., Mannell, M. V., Ling, J., Elgie, R., Gasparovic, C., Phillips, J. P., et al. (2009). Auditory orienting and inhibition of return in mild traumatic brain injury: A FMRI study. Human Brain Mapping, 30(12), 4152–4166.

  35. 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. https://doi.org/10.1002/hbm.21151.

  36. Mayer, A. R., Bellgowan, P. S., & Hanlon, F. M. (2015). Functional magnetic resonance imaging of mild traumatic brain injury. Neuroscience & Biobehavioral Reviews, 49, 8–18.

  37. Mayer, A. R., Quinn, D. K., & Master, C. L. (2017). The spectrum of mild traumatic brain injury a review. Neurology, 89(6), 623–632.

  38. McCrory, P., Meeuwisse, W. H., Aubry, M., Cantu, B., Dvorak, J., Echemendia, R. J., & Turner, M. (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. https://doi.org/10.1136/bjsports-2013-092313.

  39. McIntosh, A. R. (1999). Mapping cognition to the brain through neural interactions. Memory, 7(5–6), 523–548.

  40. McKee, A. C., & Robinson, M. E. (2014). Military-related traumatic brain injury and neurodegeneration. Alzheimer's & Dementia, 10(3), S242–S253.

  41. McKee, A. C., Cantu, R. C., Nowinski, C. J., Hedley-Whyte, E. T., Gavett, B. E., Budson, A. E., et al. (2009). Chronic traumatic encephalopathy in athletes: Progressive Tauopathy after repetitive head injury. Journal of Neuropathology and Experimental Neurology, 68(7), 709–735.

  42. McKee, A. C., Stern, R. A., Nowinski, C. J., Stein, T. D., Alvarez, V. E., Daneshvar, D. H., et al. (2013). The spectrum of disease in chronic traumatic encephalopathy. Brain, 136, 1. https://doi.org/10.1093/brain/awt051.

  43. Mendez, M. F., Owens, E. M., Reza Berenji, G., Peppers, D. C., Liang, L.-J., & Licht, E. A. (2013). Mild traumatic brain injury from primary blast vs. blunt forces: Post-concussion consequences and functional neuroimaging. NeuroRehabilitation, 32(2), 397–407.

  44. Narayan, R. K., Michel, M. E., Ansell, B., Baethmann, A., Biegon, A., Bracken, M. B., et al. (2002). Clinical trials in head injury. Journal of Neurotrauma, 19(5), 503–557.

  45. Nencka, A. S., Meier, T. B., Wang, Y., Muftuler, L. T., Wu, Y. C., Saykin, A. J., & Guskiewicz, K. M. (2018). Stability of MRI metrics in the advanced research core of the NCAA-DoD concussion assessment, research and education (CARE) consortium. Brain Imaging and Behavior, 12(4), 1121–1140.

  46. Ploughman, M. (2008). Exercise is brain food: The effects of physical activity on cognitive function. Developmental Neurorehabilitation, 11(3), 236–240. https://doi.org/10.1080/17518420801997007.

  47. Saatman, K. E., Duhaime, A.-C., Bullock, R., Maas, A. I., Valadka, A., & Manley, G. T. (2008). Classification of traumatic brain injury for targeted therapies. Journal of Neurotrauma, 25(7), 719–738.

  48. Sheline, Y. I., & Raichle, M. E. (2013). Resting state functional connectivity in preclinical Alzheimer's disease. Biological Psychiatry, 74(5), 340–347. https://doi.org/10.1016/j.biopsych.2012.11.028.

  49. Shultz, S. R., MacFabe, D. F., Foley, K. A., Taylor, R., & Cain, D. P. (2012). Sub-concussive brain injury in the long-Evans rat induces acute neuroinflammation in the absence of behavioral impairments. Behavioural Brain Research, 229(1), 145–152. https://doi.org/10.1016/j.bbr.2011.12.015.

  50. Singh, R., Meier, T. B., Kuplicki, R., Savitz, J., Mukai, I., Cavanagh, L., et al. (2014). Relationship of collegiate football experience and concussion with hippocampal volume and cognitive outcomes. Jama, 311(18), 1883–1888.

  51. Sivanandam, T. M., & Thakur, M. K. (2012). Traumatic brain injury: A risk factor for Alzheimer's disease. Neuroscience and Biobehavioral Reviews, 36(5), 1376–1381. https://doi.org/10.1016/j.neubiorev.2012.02.013.

  52. 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(2), 341–354. https://doi.org/10.1007/s00221-009-2141-6.

  53. Slobounov, S. M., 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. https://doi.org/10.1016/j.neuroimage.2011.01.024.

  54. Sripada, R. K., King, A. P., Welsh, R. C., Garfinkel, S. N., Wang, X., Sripada, C. S., & Liberzon, I. (2012). Neural dysregulation in posttraumatic stress disorder: Evidence for disrupted equilibrium between salience and default mode brain networks. Psychosomatic Medicine, 74(9), 904–911.

  55. Stern, R. A., Riley, D. O., Daneshvar, D. H., Nowinski, C. J., Cantu, R. C., & McKee, A. C. (2011). Long-term consequences of repetitive brain trauma: Chronic traumatic encephalopathy. Pm&R, 3(10), S460–S467. https://doi.org/10.1016/j.pmrj.2011.08.008.

  56. Talavage, T. M., Nauman, E., Breedlove, E. L., Yoruk, U., Dye, A. E., Morigaki, K., et al. (2010). Functionally-detected cognitive impairment in high school football players without clinically-diagnosed concussion. Journal of Neurotrauma, 31, 327–338. https://doi.org/10.1089/neu.2010.1512.

  57. Vagnozzi, R., Tavazzi, B., Signoretti, S., Amorini, A. M., Belli, A., Cimatti, M., et al. (2007). Temporal window of metabolic brain vulnerability to concussions: Mitochondrial-related impairment - part I. Neurosurgery, 61(2), 379–388. https://doi.org/10.1227/01.neu.0000280002.41696.d8.

  58. Vagnozzi, R., Signoretti, S., Cristofori, L., Alessandrini, F., Floris, R., Isgro, E., . . . Tavazzi, B. (2010). Assessment of metabolic brain damage and recovery following mild traumatic brain injury: A multicentre, proton magnetic resonance spectroscopic study in concussed patients. Brain, 133(11), 3232–3242.

  59. Vagnozzi, R., Signoretti, S., Floris, R., Marziali, S., Manara, M., Amorini, A. M., et al. (2013). Decrease in N-acetylaspartate following concussion may be coupled to decrease in creatine. The Journal of Head Trauma Rehabilitation, 28(4), 284–292.

  60. Yarrow, K., Brown, P., & Krakauer, J. W. (2009). Inside the brain of an elite athlete: The neural processes that support high achievement in sports. Nature Reviews Neuroscience, 10(8), 585–596.

  61. Yoo, K., Sohn, W. S., & Jeong, Y. (2013). Tool-use practice induces changes in intrinsic functional connectivity of parietal areas. Frontiers in Human Neuroscience, 7, 49.

  62. Zhu, D. C., Covassin, T., Nogle, S., Doyle, S., Russell, D., Pearson, R. L., et al. (2015). A potential biomarker in sports-related concussion: Brain functional connectivity alteration of the default-mode network measured with longitudinal resting-state fMRI over thirty days. Journal of Neurotrauma, 32(5), 327–341.

  63. Zohar, O., Lavy, R., Zi, X. M., Nelson, T. J., Hongpaisan, J., Pick, C. G., & Alkon, D. L. (2011). PKC activator therapeutic for mild traumatic brain injury in mice. Neurobiology of Disease, 41(2), 329–337. https://doi.org/10.1016/j.nbd.2010.10.001.

Download references

Author information

Correspondence to Semyon Slobounov.

Additional information

The original version of this article was revised: The article title should be “Are there any differential responses to concussive injury in civilian versus athletic populations: a neuroimaging study”.

Electronic supplementary material


(PDF 373 kb)


(DOCX 16 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Johnson, B., Dodd, A., Mayer, A.R. et al. Are there any differential responses to concussive injury in civilian versus athletic populations: a neuroimaging study. Brain Imaging and Behavior 14, 110–117 (2020). https://doi.org/10.1007/s11682-018-9982-1

Download citation


  • Concussion
  • Mild traumatic brain injury (mTBI)
  • Resting state functional magnetic resonance imaging (rs-fMRI)
  • Default mode network (DMN)