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Theta-Band Functional Connectivity and Single-Trial Cognitive Control in Sports-Related Concussion: Demonstration of Proof-of-Concept for a Potential Biomarker of Concussion

  • Ezra E. Smith (a1) and John J.B. Allen (a1)

Abstract

Objectives: This report examined theta-band neurodynamics for potential biomarkers of brain health in athletes with concussion. Methods: Participants included college-age contact/collision athletes with (N=24) and without a history of concussion (N=16) in Study 1. Study 2 (N=10) examined changes over time in contact/collision athletes. There were two primary dependent variables: (1) theta-band phase-synchronization (e.g., functional connectivity) between medial and right-lateral electrodes; and (2) the within-subject correlation between synchronization strength on error trials and post-error reaction time (i.e., operationalization of cognitive control). Results: Head injury history was inversely related with medial-lateral connectivity. Head injury was also related to declines in a neurobehavioral measure of cognitive control (i.e., the single-trial relationship between connectivity and post-error slowing). Conclusions: Results align with a theory of connectivity-mediated cognitive control. Mild injuries undetectable by behavioral measures may still be apparent on direct measures of neural functioning. This report demonstrates that connectivity and cognitive control measures may be useful for tracking recovery from concussion. Theoretically relevant neuroscientific findings in healthy adults may have applications in patient populations, especially with regard to monitoring brain health. (JINS 2019, 25, 314–323)

Copyright

Corresponding author

Correspondence and reprint requests to: Ezra E. Smith, University of Arizona, Department of Psychology, 1503 E. University Blvd., Tucson, AZ 85721. E-mail: ezrasmith@email.arizona.edu

References

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Aron, A.R., Robbins, T.W., & Poldrack, R.A. (2014). Inhibition and the right inferior frontal cortex: one decade on. Trends in cognitive sciences, 18(4), 177185.
Bailey, N.W., Rogasch, N.C., Hoy, K.E., Maller, J.J., Segrave, R.A., Sullivan, C.M., & Fitzgerald, P.B. (2017). Increased gamma connectivity during working memory retention following traumatic brain injury. Brain Injury, 31(3), 379389.
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society . Series B, Statistical Methodology, 57, 289300.
Bigler, E.D. (2007). Anterior and middle cranial fossa in traumatic brain injury: Relevant neuroanatomy and neuropathology in the study of neuropsychological outcome. Neuropsychology, 21(5), 515.
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(1), 1623.
Broglio, S.P., Pontifex, M.B., O'Connor, P., & Hillman, C.H. (2009). The persistent effects of concussion on neuroelectric indices of attention. Journal of neurotrauma, 26(9), 14631470.
Buzsáki, G. (2006). Rhythms of the brain. New York: Oxford University Press.
Buzzell, G.A., Barker, T.V., Troller-Renfree, S.V., Bernat, E.M., Bowers, M.E., MoralesS.,. S.,. & Fox, N.A. (2018). Adolescent cognitive control, theta oscillations, and social motivation. bioRxiv, doi: https://doi.org/10.1101/366831
Cavanagh, J.F., Cohen, M.X., & Allen, J.J. (2009). Prelude to and resolution of an error: EEG phase synchrony reveals cognitive control dynamics during action monitoring. The Journal of Neuroscience, 29(1), 98105.
Cavanagh, J.F., & Frank, M.J. (2014). Frontal theta as a mechanism for cognitive control. Trends in Cognitive Sciences, 18(8), 414421.
Cavanagh, J.F., Frank, M.J., Klein, T.J., & Allen, J.J. (2010). Frontal theta links prediction errors to behavioral adaptation in reinforcement learning. Neuroimage, 49(4), 31983209.
Cavanagh, J.F., Meyer, A., & Hajcak, G. (2017). Error-specific cognitive control alterations in generalized anxiety disorder. Biological Psychiatry. Cognitive Neuroscience and Neuroimaging, 2(5), 413420.
Cavanagh, J.F., & Shackman, A.J. (2015). Frontal midline theta reflects anxiety and cognitive control: Meta-analytic evidence. Journal of Physiology, Paris, 109(1), 315.
Cavanagh, J.F., Zambrano‐Vazquez, L., & Allen, J.J. (2012). Theta lingua franca: A common mid‐frontal substrate for action monitoring processes. Psychophysiology, 49(2), 220238.
Cohen, M.X. (2011a). Error-related medial frontal theta activity predicts cingulate-related structural connectivity. Neuroimage, 55(3), 13731383.
Cohen, M.X. (2011b). It’s about time. Frontiers in Human Neuroscience, 5, 2.
Cohen, M.X. (2014). Analyzing neural time series data: Theory and practice. Cambridge: MIT Press.
Cohen, M.X., & Cavanagh, J.F. (2011). Single-trial regression elucidates the role of prefrontal theta oscillations in response conflict. Frontiers in Psychology, 2, 30.
Cohen, J., & Cohen, P. (1983). Applied multiple regression/correlation analysis for the behavioral sciences. Mahwah NJ: Erlbaum.
Cohen, M.X., & van Gaal, S. (2013). Dynamic interactions between large-scale brain networks predict behavioral adaptation after perceptual errors. Cerebral Cortex, 23(5), 10611072.
Cook, E.W., & Miller, G.A. (1992). Digital filtering: Background and tutorial for psychophysiologists. Psychophysiology, 29(3), 350362.
Coronado, V.G., McGuire, L.C., Sarmiento, K., Bell, J., Lionbarger, M.R., Jones, C.D., . . . Xu, L. (2012). Trends in traumatic brain injury in the U.S. and the public health response: 1995–2009. Journal of Safety Research, 43(4), 299307.
De Beaumont, L., Beauchemin, M., Beaulieu, C., & Jolicoeur, P. (2013). Long-term attenuated electrophysiological response to errors following multiple sports concussions. Journal of Clinical and Experimental Neuropsychology, 35(6), 596607.
Debener, S., Ullsperger, M., Siegel, M., Fiehler, K., Von Cramon, D.Y., & Engel, A.K. (2005). Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring. The Journal of Neuroscience, 25(50), 1173011737.
Duncan, C.C., Kosmidis, M.H., & Mirsky, A.F. (2003). Event-related potential assessment of information processing after closed head injury. Psychophysiology, 40(1), 4559.
Eierud, C., Craddock, R.C., Fletcher, S., Aulakh, M., King-Casas, B., Kuehl, D., & LaConte, S.M. (2014). Neuroimaging after mild traumatic brain injury: Review and meta-analysis. NeuroImage. Clinical, 4, 283294.
Faul, M., Xu, L., Wald, M.M., & Coronado, V.G. (2010). Traumatic brain injury in the United States: Emergency department visits, hospitalizations, and deaths. Atlanta: Centers for Disease Control and Prevention. National Center for Injury Prevention and Control.
Fries, P. (2005). A mechanism for cognitive dynamics: Neuronal communication through neuronal coherence. Trends in Cognitive Sciences, 9(10), 474480.
Gehring, W.J., Goss, B., Coles, M.G., Meyer, D.E., & Donchin, E. (1993). A neural system for error detection and compensation. Psychological Science, 4(6), 385390.
Gehring, W.J., & Knight, R.T. (2000). Prefrontal-cingulate interactions in action monitoring. Nature Neuroscience, 3(5), 516.
Hajcak, G., McDonald, N., & Simons, R.F. (2003). To err is autonomic: Error‐related brain potentials, ANS activity, and post‐error compensatory behavior. Psychophysiology, 40(6), 895903.
Hill, K.E., Samuel, D.B., & Foti, D. (2016). Contextualizing individual differences in error monitoring: Links with impulsivity, negative affect, and conscientiousness. Psychophysiology, 53(8), 11431153.
Hogan, A.M., Vargha-Khadem, F., Saunders, D.E., Kirkham, F.J., & Baldeweg, T. (2006). Impact of frontal white matter lesions on performance monitoring: ERP evidence for cortical disconnection. Brain, 129(8), 21772188.
Iverson, G.L., Wojtowicz, M., Brooks, B.L., Maxwell, B.A., Atkins, J.E., Zafonte, R., & Berkner, P.D. (2016). High school athletes with ADHD and learning difficulties have a greater lifetime concussion history. Journal of Attention Disorders, 1, 17.
Karr, J.E., Areshenkoff, C.N., & Garcia-Barrera, M.A. (2014). The neuropsychological outcomes of concussion: A systematic review of meta-analyses on the cognitive sequelae of mild traumatic brain injury. Neuropsychology, 28(3), 321.
Kerns, J.G., Cohen, J.D., MacDonald, A.W., Cho, R.Y., Stenger, V.A., & Carter, C.S. (2004). Anterior cingulate conflict monitoring and adjustments in control. Science, 303(5660), 10231026.
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(5), 665675.
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 and Rehabilitation, 21(5), 375378.
Larson, M.J., Clayson, P.E., & Farrer, T.J. (2012). Performance monitoring and cognitive control in individuals with mild traumatic brain injury. Journal of the International Neuropsychological Society, 18(2), 323.
Larson, M.J., Farrer, T.J., & Clayson, P.E. (2011). Cognitive control in mild traumatic brain injury: Conflict monitoring and conflict adaptation. International Journal of Psychophysiology, 82(1), 6978.
McCrory, P., Meeuwisse, W., Johnston, K., Dvorak, J., Aubry, M., Molloy, M., & Cantu, R. (2009). Consensus statement on concussion in sport 3rd International Conference on Concussion in Sport held in Zurich, November 2008. British Journal of Sports Medicine, 19(3), 185200.
Miller, D.R., Hayes, J.P., Lafleche, G., Salat, D.H., & Verfaellie, M. (2017). White matter abnormalities are associated with overall cognitive status in blast-related mTBI. Brain Imaging and Behavior, 11(4), 11291138.
Mognon, A., Jovicich, J., Bruzzone, L., & Buiatti, M. (2011). ADJUST: An automatic EEG artifact detector based on the joint use of spatial and temporal features. Psychophysiology, 48(2), 229240.
Moore, R.D., Pindus, D.M., Drolette, E.S., Scudder, M.R., Raine, L.B., & Hillman, C.H. (2015). The persistent influence of pediatric concussion on attention and cognitive control during flanker performance. Biological Psychology 109, 93102.
Narayanan, N.S., Cavanagh, J.F., Frank, M.J., & Laubach, M. (2013). Common medial frontal mechanisms of adaptive control in humans and rodents. Nature. Neuroscience, 16(12), 1888.
Nieuwenhuis, S., Ridderinkhof, K.R., Blom, J., Band, G.P., & Kok, A. (2001). Error‐related brain potentials are differentially related to awareness of response errors: Evidence from an antisaccade task. Psychophysiology, 38(5), 752760.
Olvet, D.M., & Hajcak, G. (2009). Reliability of error-related brain activity. Brain Research, 1284, 8999.
Olvet, D.M., Klein, D.N., & Hajcak, G. (2010). Depression symptom severity and error-related brain activity. Psychiatry Research, 179(1), 3037.
Orr, C.A., Albaugh, M.D., Watts, R., Garavan, H., Andrews, T., Nickerson, J.P., . . . Hudziak, J.J. (2016). Neuroimaging biomarkers of a history of concussion observed in asymptomatic young athletes. Journal of Neurotrauma, 33(9), 803.
Pang, E.W., Dunkley, B.T., Doesburg, S.M., da Costa, L., & Taylor, M.J. (2016). Reduced brain connectivity and mental flexibility in mild traumatic brain injury. Annals of Clinical and Translational Neurology, 3(2), 124131.
Perrin, F., Pernier, J., Bertrand, O., Echallier, J.F., 1989. Spherical splines for scalp potential and current density mapping. Electroencephalography and Clinical Neurophysiology, 72, 184187.
Perrin, F., Pernier, J., Bertrand, O., & Echallier, J.F. 1990. Corrigenda. Electroencephalography and Clinical Neurophysiology, 76, 565566.
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(14), 32103216.
Polich, J. (2007). Updating P300: An integrative theory of P3a and P3b. Clinical Neurophysiology, 118(10), 21282148.
Riesel, A., Weinberg, A., Endrass, T., Meyer, A., & Hajcak, G. (2013). The ERN is the ERN is the ERN? Convergent validity of error-related brain activity across different tasks. Biological Psychology, 93(3), 377385.
Reches, A., Kutcher, J., Elbin, R.J., Or-Ly, H., Sadeh, B., Greer, J., . . . Kontos, A.P. (2017). Preliminary investigation of Brain Network Activation (BNA) and its clinical utility in sport-related concussion. Brain Injury, 31(2), 237246.
Rutland-Brown, W., Langlois, J.A., Thomas, K.E., & Xi, Y.L. (2006). Incidence of traumatic brain injury in the United States, 2003. The Journal of Head Trauma Rehabilitation, 21(6), 544548.
Smith, E.E., Reznik, S.J., Stewart, J.L., & Allen, J.J. (2017). Assessing and conceptualizing frontal EEG asymmetry: An updated primer on recording, processing, analyzing, and interpreting frontal alpha asymmetry. International Journal of Psychophysiology, 111, 98114.
Sponheim, S.R., McGuire, K.A., Kang, S.S., Davenport, N.D., Aviyente, S., Bernat, E.M., & Lim, K.O. (2011). Evidence of disrupted functional connectivity in the brain after combat-related blast injury. Neuroimage, 54, S21S29.
Stemmer, B., Segalowitz, S.J., Witzke, W., & Schönle, P.W. (2004). Error detection in patients with lesions to the medial prefrontal cortex: An ERP study. Neuropsychologia, 42(1), 118130.
Tsirka, V., Simos, P.G., Vakis, A., Kanatsouli, K., Vourkas, M., Erimaki, S., . . . Micheloyannis, S. (2011). Mild traumatic brain injury: Graph-model characterization of brain networks for episodic memory. International Journal of Psychophysiology, 79(2), 8996.
Ullsperger, M., & von Cramon, D.Y. (2006). The role of intact frontostriatal circuits in error processing. Journal of Cognitive Neuroscience, 18(4), 651664.
Van de Vijver, I., Ridderinkhof, K.R., & Cohen, M.X. (2011). Frontal oscillatory dynamics predict feedback learning and action adjustment. Journal of Cognitive Neuroscience, 23(12), 41064121.
Wessel, J.R., Klein, T.A., Ott, D.V., & Ullsperger, M. (2014). Lesions to the prefrontal performance-monitoring network disrupt neural processing and adaptive behaviors after both errors and novelty. Cortex, 50, 4554.
Wessel, J.R., Ullsperger, M., Obrig, H., Villringer, A., Quinque, E., Schroeter, M.L., . . . & Klein, T.A. (2016). Neural synchrony indexes impaired motor slowing after errors and novelty following white matter damage. Neurobiology of Aging, 38, 205213.
Wessel, J.R. (2018). An adaptive orienting theory of error processing. Psychophysiology, 55(3). doi:10.1111/psyp.13041
Zambrano-Vazquez, L., & Allen, J.J. (2014). Differential contributions of worry, anxiety, and obsessive compulsive symptoms to ERN amplitudes in response monitoring and reinforcement learning tasks. Neuropsychologia, 61, 197209.
Zelazo, P.D., Anderson, J.E., Richler, J., Wallner-Allen, K., Beaumont, J.L., Conway, K.P., . . . Weintraub, S. (2014). NIH Toolbox Cognition Battery (CB): Validation of executive function measures in adults. Journal of the International Neuropsychological Society, 20(6), 620629.

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