Skip to main content
SpringerLink
Log in

Neurophysiological correlates of persistent psycho-affective alterations in athletes with a history of concussion

  • Original Research
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

Understanding the neuropathological underpinnings of sport-related concussion are critical for diagnosis, prognosis, and remediation. Although electro-encephalographic (EEG) methods have proven invaluable for understanding psycho-affective pathologies in various clinical conditions, they have not been used to understand the psycho-affective outcomes of concussive injuries. Accordingly, we evaluated the relation of electroencephalographic (EEG) power in collegiate athletes to psycho-affective measures. We predicted that athletes with a history of concussion would exhibit alterations in frontal EEG asymmetries indicative of increased depression, anxiety and more general mood disturbance. During this cross-sectional study, resting EEG and measures of mood and affect, including the Beck Depression Inventory-II (BDI-II) and Profile of Mood States (POMS) were collected in 81 young-adult male athletes (52 concussion history; 29 controls). All athletes with a history of concussion (9+ months from injury) reported to be symptom free, and all participants were actively taking part in their sport at the time of testing. Compared to control athletes, the athletes with a history of concussion exhibited alterations in frontal-alpha and frontal-beta asymmetry (p’s < .05). Correlational analyses revealed that alterations in frontal-alpha asymmetry were related to self-reported depression and anxiety, and alterations in beta-asymmetry were related to self-reported anger/aggression, but these relations were only significant for athletes with a history of concussion. The current study suggests that athletes with a history of concussion who made a complete return to play and reported to be asymptomatic on a commonly used symptom checklist may still exhibit neural activity associated with increased levels of depression, anxiety and anger/hostility. The current results reinforce the clinical necessity for long-term evaluations of athletes irrespective of apparent symptom resolution, and suggest that EEG may serve as a sensitive tool to identify and track concussion-related alterations in psycho-affective health before they manifest as clinical disorders.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alhilali, L. M., Delic, J. A., Gumus, S., & Fakhran, S. (2015). Evaluation of white matter injury patterns underlying neuropsychiatric symptoms after mild traumatic brain injury. Radiology. doi:10.1148/radiol.2015142974.

  • Allen, J. J. B., & Kline, J. P. (2004). Frontal EEG asymmetry, emotion, and psychopathology: the first, and the next, twenty-five years. Biological Psychology, 67, 1–5.

    Article  PubMed  Google Scholar 

  • American Academy of Neurology (1997). AAN practice parameter: The management of concussion in sports (summary statement). Report of the Quality Standards Subcommittee. Neurology, 48, 581–585.

    Article  Google Scholar 

  • Baillargeon, A., Lassonde, M., Leclerc, S., & Ellemberg, D. (2012). Neuropsychological and neurophysiological assessment of sport concussion in children, adolescents and adults. Brain Injury, 26, 211–220.

    Article  PubMed  Google Scholar 

  • Baugh, C. M., Stamm, J. M., Riley, D. O., et al. (2012). Chronic traumatic encephalopathy: neurodegeneration following repetitive concussive and subconcussive brain trauma. Brain Imaging Behavior, 6, 244–254.

    Article  PubMed  Google Scholar 

  • Beck, A. T., Steer, R. A., Beck, J. S., & Newman, C. F. (1993). Hopelessness, depression, suicidal ideation, and clinical diagnosis of depression. Suicide & Life-Threatening Behavior, 23, 139–145.

    CAS  Google Scholar 

  • Bigler, E. D., & Maxwell, W. L. (2012). Neuropathology of mild traumatic brain injury: relationship to neuroimaging findings. Brain Imaging Behavior, 6(2), 108–136.

    Article  PubMed  Google Scholar 

  • Blackhart, G. C., Minnix, J. A., & Kline, J. P. (2006). Can eeg asymmetry patterns predict future development of anxiety and depression? A preliminary study. Biological Psychology, 72, 46–50.

    Article  PubMed  Google Scholar 

  • Broglio, S. P., Sosnoff, J. J., & Ferrara, M. S. (2009). The relationship of athlete-reported concussion symptoms and objective measures of neurocognitive function and postural control. Clinical Journal of Sport Medicine, 19, 377–382.

    Article  PubMed  Google Scholar 

  • Broglio, S. P., Moore, R. D., & Hillman, C. H. (2011). A history of sport-related concussion on event-related brain potential correlates of cognition. International Journal of Psychophysiology, 82, 16–23.

    Article  PubMed  Google Scholar 

  • Chen, J. K., Johnston, K. M., Frey, S., et al. (2004). Functional abnormalities in symptomatic concussed athletes: an fMRI study. NeuroImage, 22(1), 68–82.

    Article  PubMed  Google Scholar 

  • Chen, J. K., Johnston, K. M., Collie, A., et al. (2007). A validation of the post concussion symptom scale in the assessment of complex concussion using cognitive testing and functional MRI. Journal of Neurology, Neurosurgery and Psychiatry., 78, 1231–1238.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen, J. K., Johnston, K. M., Petrides, M., & Ptito, A. (2008). Neural substrates of symptoms of depression following concussion in male athletes with persisting postconcussion symptoms. Archives of General Psychiatry, 65(1), 81–89.

    Article  PubMed  Google Scholar 

  • Coan, J. A., & Allen, J. J. (2004). Frontal EEG asymmetry as a moderator and mediator of emotion. Biological Psychology, 67, 7–49.

    Article  PubMed  Google Scholar 

  • Cook, I. A., Hunter, A. M., Abrams, M., Siegman, B., & Leuchter, A. F. (2009). Midline and right frontal brain function as a physiologic biomarker of remission in major depression. Psychiatry Research, 174, 152–157.

    Article  PubMed  PubMed Central  Google Scholar 

  • Curran, S. L., Sherman, J. J., Cunningham, L. L., Okeson, J. P., Reid, K. I., & Carlson, C. R. (1995). Physical and sexual abuse among orofacial pain patients: linkages with pain and psychologic distress. Journal of Orofacial Pain, 9, 340–346.

    CAS  PubMed  Google Scholar 

  • Daneshvar, D. H., Nowinski, C. J., McKee, A. C., & Cantu, R. C. (2011). The epidemiology of sport-related concussion. Clinics in Sports Medicine, 30, 1–17.

    Article  PubMed  PubMed Central  Google Scholar 

  • Davidson, R. J. (1992). Anterior cerebral asymmetry and the nature of emotion. Brain & Cognition, 20, 125–151.

    Article  CAS  Google Scholar 

  • Davidson, R. J. (2002). Anxiety and affective style: role of prefrontal cortex and amygdala. Biological Psychiatry, 5, 68–80.

    Article  Google Scholar 

  • Davidson, R. J. (2004). What does the prefrontal cortex “do” in affect: perspectives on frontal eeg asymmetry research. Biological Psychology, 67, 219–233.

    Article  PubMed  Google Scholar 

  • Davidson, R. J., & Sutton, S. K. (1995). Affective neuroscience: the emergence of a discipline. Current Opinion in Neurobiology, 5, 217–224.

    Article  CAS  PubMed  Google Scholar 

  • Davidson, R. J., Jackson, D. C., & Larson, C. L. (2000). Human electroencephalography. In J. T. Cacciopo, L. G. Tassinary, & G. G. Berntson (Eds.), Handbook of psychophysiology (vol. 2, 2nd ed., pp. 27–52). Cambridge: Cambridge University Press.

    Google Scholar 

  • Ellemberg, D., Leclerc, S., Couture, S., & Daigle, C. (2007). Prolonged neuropsychological impairments following a first concussion in female university soccer athletes. Clinical Journal of Sport Medicine, 17, 369–374.

    Article  PubMed  Google Scholar 

  • Gaetz, M., Goodman, D., & Weinberg, H. (2000). Electrophysiological evidence for the cumulative effects of concussion. Brain Injury, 14, 1077–1088.

    Article  CAS  PubMed  Google Scholar 

  • Gosselin, N., Bottari, C., Ptito, A., et al. (2012). Evaluating the cognitive consequences of mild traumatic brain injury and concussion by using electrophysiology. Neurosurgical Focus, 33(E7), 1–7.

    Google Scholar 

  • Grimshaw, G. M., & Carmel, D. (2014). An asymmetric inhibition model of hemispheric differences in emotional processing. Frontiers in Psychology, 5, 489.

    Article  PubMed  PubMed Central  Google Scholar 

  • Guskiewicz, K. M., Marshall, S. W., & Cantu, R. C. (2007). Recurrent concussion and risk of depression in retired professional football players. Medicine and Science in Sports and Exercise, 39, 903–909.

    Article  PubMed  Google Scholar 

  • Harmon-Jones, E. (2007). Asymmetrical frontal cortical activity, affective valence, and motivational direction. In E. Harmon-Jones, & P. Winkielman (Eds.), Social neuroscience: Integrating biological and psychological explanations of social behavior (1st ed., pp. 137–156). New York: Guilford Publications.

    Google Scholar 

  • Harmon-Jones, E., & Allen, J. J. B. (1997). Behavioral activation sensitivity and resting frontal EEG asymmetry: covariation of putative indicators related to risk for mood disorders. Journal of Abnormal Psychology, 106(1), 159.

    Article  CAS  PubMed  Google Scholar 

  • Harmon-Jones, E., & Peterson, C. K. (2009). Electroencephalographic methods. In E. Harmon-Jones, & J. S. Beer (Eds.), Methods in social neuroscience (2nd ed., pp. 170–197). New York: Guilford Publications.

    Google Scholar 

  • Harmon-Jones, E., Gable, P. A., & Peterson, C. K. (2010). The role of asymmetric frontal cortical activity in emotion-related phenomena: a review and update. Biological Psychology, 84, 451–462.

    Article  PubMed  Google Scholar 

  • Hofman, D., & Schutter, D. J. (2012). Asymmetrical frontal resting-state beta oscillations predict trait aggressive tendencies and behavioral inhibition. Social Cognitive and Affective Neuroscience, 7, 850–857.

    Article  PubMed  Google Scholar 

  • Kerr, Z. Y., Marshall, S. W., Harding, H. P., & Guskiewicz, K. M. (2012). Nine-year risk of depression diagnosis increases with increasing self-reported concussions in retired professional football players. The American Journal of Sports Medicine, 40, 2206–2212.

    Article  PubMed  Google Scholar 

  • Lang, P. J., & Bradley, M. M. (2010). Emotion and the motivational brain. Biological Psychology, 84, 437–450.

    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, 375–378.

    Article  PubMed  Google Scholar 

  • Lipton, M. L., Kim, N., Lipton, R. B., et al. (2012). Robust detection of traumatic axonal injury in individual mild traumatic brain injury patients: intersubject variation, change over time and bidirectional changes in anisotropy. Brain Imaging Behavior, 6, 329–342.

    Article  PubMed  Google Scholar 

  • Mainwaring, L. M., Bisschop, S. M., Richards, D. W., et al. (2004). Emotional reaction of varsity athletes to sport-related concussion. Journal of Sport & Exercise Psychology, 26, 119–135.

    Article  Google Scholar 

  • Mainwaring, L., Hutchison, M., Comper, P., Richards, D., & Trenerry, M. (2012). Examining emotional sequelae of sport concussion. Journal of Clinical Sport Psychology, 6, 247.

    Article  Google Scholar 

  • Mayer, A. R., Yang, Z., et al. (2012). A functional MRI study of multimodal selective attention following mild traumatic brain injury. Brain Imaging Behavior, 6, 343–354.

    Article  PubMed  Google Scholar 

  • McCrory, P., Meeuwisse, W., Cantu, R. C., et al. (2009). Consensus statement on concussion in sport–the 3rd international conference on concussion in sport held in Zurich, November 2008. South African Journal of Sports Medicine, 21, 36–46.

    Article  Google Scholar 

  • McKee, A., Stern, R., Cantu, R. C., et al. (2012). The spectrum of disease in chronic traumatic encephalopathy. Brain, 136, 43–64.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mooney, G., & Speed, J. (2001). The association between mild traumatic brain injury and psychiatric conditions. Brain Injury, 15, 865–877.

    Article  CAS  PubMed  Google Scholar 

  • Moore, R. D., Hillman, C. H., & Broglio, S. P. (2014). The persistent influence of concussive injuries on cognitive control and neuroelectric function. Journal of Athletic Training, 49, 24–35.

    Article  PubMed  PubMed Central  Google Scholar 

  • Niogi, S., Mukherjee, P., Ghajar, J., et al. (2010). Individual differences in distinct components of attention are linked to anatomical variations in distinct white matter tracts. Frontiers in Neuroanatomy, 4, 2.

    PubMed  PubMed Central  Google Scholar 

  • Nusslock, R., Shackman, A. J., Harmon-Jones, E., et al. (2011). Cognitive vulnerability and frontal brain asymmetry: common predictors of first prospective depressive episode. Journal of Abnormal Psychology, 120, 497.

    Article  PubMed  PubMed Central  Google Scholar 

  • Plutchik, R. (1994). The psychology and biology of emotion. New York: HarperCollins College Publishers.

    Google Scholar 

  • Pontifex, M. B., O'Connor, P. M., Broglio, S. P., & Hillman, C. H. (2009). The association between mild traumatic brain injury history and cognitive control. Neuropsychologia, 47, 3210–3216.

    Article  PubMed  Google Scholar 

  • Rigotti, M., Barak, O., & Miller, E. K. (2013). The importance of mixed selectivity in complex cognitive tasks. Nature, 497, 585–590.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sauvé, W., Moore, R. D., & Ellemberg, D. (2015). Long-term psycho-affective outcomes of concussion in active male athletes. In press.

  • Schmitt, B. M., Munte, T. F., & Kutas, M. (2000). Electrophysiological estimates of the time course of semantic and phonological encoding during implicit picture naming. Psychophysiology, 37(4), 473–484.

    Article  CAS  PubMed  Google Scholar 

  • Sinopoli, K. J., Chen, J., Keightley, M. L., et al. (2014). Imaging “brain strain” in youth athletes with mild traumatic brain injury during dual-task performance. Journal of Neurotrauma, 31, 1843–1859.

    Article  PubMed  Google Scholar 

  • Slobounov, S., Gay, M., Johnson, B., & Zhang, K. (2012). Concussion in athletics: ongoing clinical and brain imaging research controversies. Brain Imaging Behavior, 6, 224–243.

    Article  PubMed  Google Scholar 

  • Urban, K. J., Barlow, K. M., Jimenez, J. J., Goodyear, B. G., & Dunn, J. F. (2015). Functional near-infrared spectroscopy reveals reduced interhemispheric cortical communication after pediatric concussion. Journal of Neurotrauma, 32, 833–840.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vargas, G., Rabinowitz, A., Meyer, J., & Arnett, P. A. (2015). Predictors and prevalence of postconcussion depression symptoms in collegiate athletes. Journal of Athletic Training, 50, 250–255.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang, K., Johnson, B., Slobounov, S., et al. (2012). Default mode network in concussed individuals in response to the YMCA physical stress test. Journal of Neurotrauma, 29, 756–765.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. University of Montreal, Montreal, QC, Canada

    Robert Davis Moore, William Sauve & Dave Ellemberg

Authors
  1. Robert Davis Moore
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. William Sauve
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dave Ellemberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Robert Davis Moore.

Ethics declarations

Funding

This study was funded by a Canadian Institute of Health Research grant (#R0017986), awarded to Dave Ellemberg.

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all participants included in the study.

Additional information

What is known about the subject: Concussive injuries can lead to persistent alterations in aspects of neurophysiological function essential to cognition and motor function. However, little is known regarding the outcomes of concussive injuries on psycho-affective mood states, and the neural substrates supporting them.

What this study adds to existing knowledge: The current study adds important information regarding the long-term outcomes of concussion on psycho-affective states. Specifically, the current study is the first to describe the EEG correlates of psycho-affective perturbations in active athletes with a history of concussion. In doing so, the data indicate that asymptomatic athletes far removed from injury still exhibit abnormal neural activity associated with increased levels of depression, anxiety and anger/aggression. The current study also demonstrates the clinical utility of evaluating asymmetric EEG activity for enhancing the identification and tracking of concussion-related psycho-affective alterations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moore, R.D., Sauve, W. & Ellemberg, D. Neurophysiological correlates of persistent psycho-affective alterations in athletes with a history of concussion. Brain Imaging and Behavior 10, 1108–1116 (2016). https://doi.org/10.1007/s11682-015-9473-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-015-9473-6

Keywords

Search

Navigation