Abstract
Post-traumatic migraine (PTM) (i.e., headache, nausea, light and/or noise sensitivity) is an emerging risk factor for prolonged recovery following concussion. Concussions and migraine share similar pathophysiology characterized by specific ionic imbalances in the brain. Given these similarities, patients with PTM following concussion may exhibit distinct electrophysiological patterns, although researchers have yet to examine the electrophysiological brain activation in patients with PTM following concussion. A novel approach that may help differentiate brain activation in patients with and without PTM is brain network activation (BNA) analysis. BNA involves an algorithmic analysis applied to multichannel EEG-ERP data that provides a network map of cortical activity and quantitative data during specific tasks. A prospective, repeated measures design was used to evaluate BNA (during Go/NoGo task), EEG-ERP, cognitive performance, and concussion related symptoms at 1, 2, 3, and 4 weeks post-injury intervals among athletes with a medically diagnosed concussion with PTM (n = 15) and without (NO-PTM) (n = 22); and age, sex, and concussion history matched controls without concussion (CONTROL) (n = 20). Participants with PTM had significantly reduced BNA compared to NO-PTM and CONTROLS for Go and NoGo components at 3 weeks and for NoGo component at 4 weeks post-injury. The PTM group also demonstrated a more prominent deviation of network activity compared to the other two groups over a longer period of time. The composite BNA algorithm may be a more sensitive measure of electrophysiological change in the brain that can augment established cognitive assessment tools for detecting impairment in individuals with PTM.
Similar content being viewed by others
References
Baillargeon, A., Lassonde, M., Leclerc, S., & Ellemberg, D. (2012). Neuropsychological and neurophysiological assessment of sport concussion in children, adolescents and adults. Brain Injury, 26(3), 211–220. doi:10.3109/02699052.2012.654590.
Brier, M. R., Ferree, T. C., Maguire, M. J., Moore, P., Spence, J., Tillman, G. D., et al. (2010). Frontal theta and alpha power and coherence changes are modulated by semantic complexity in Go/NoGo tasks. International Journal of Psychophysiology, 78(3), 215–224. doi:10.1016/j.ijpsycho.2010.07.011.
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), 1463–1470. doi:10.1089/neu.2008-0766.
Bullmore, E., & Sporns, O. (2009). Complex brain networks: graph theoretical analysis of structural and functional systems. Nature Reviews Neuroscience, 10(3), 186–198. doi:10.1038/nrn2575.
Buodo, G., Palomba, D., Sarlo, M., Naccarella, C., & Battistella, P. A. (2004). Auditory event-related potentials and reaction times in migraine children. Cephalalgia, 24(7), 554–563. doi:10.1111/j.1468-2982.2003.00716.x.
Buzsaki, G., & Draguhn, A. (2004). Neuronal oscillations in cortical networks. Science, 304(5679), 1926–1929. doi:10.1126/science.1099745.
Chen, W., Shen, X., Liu, X., Luo, B., Liu, Y., Yu, R., et al. (2007). Passive paradigm single-tone elicited ERPs in tension-type headaches and migraine. Cephalalgia, 27(2), 139–144. doi:10.1111/j.1468-2982.2006.01256.x.
Collins, M. W., Iverson, G. L., Lovell, M. R., McKeag, D. B., Norwig, J., & Maroon, J. (2003). On-field predictors of neuropsychological and symptom deficit following sports-related concussion. Clinical Journal of Sport Medicine, 13(4), 222–229.
Coppola, G., Cremers, J., Gerard, P., Pierelli, F., & Schoenen, J. (2011). Effects of light deprivation on visual evoked potentials in migraine without aura. BMC Neurology, 11, 91. doi:10.1186/1471-2377-11-91.
Coppola, G., Parisi, V., Di Lorenzo, C., Serrao, M., Magis, D., Schoenen, J., et al. (2013). Lateral inhibition in visual cortex of migraine patients between attacks. Journal of Headache and Pain, 14(1), 20. doi:10.1186/1129-2377-14-20.
Covassin, T., Elbin, R. J., Harris, W., Parker, T., & Kontos, A. (2012). The role of age and sex in symptoms, neurocognitive performance, and postural stability in athletes after concussion. American Journal of Sports Medicine, 40(6), 1303–1312. doi:10.1177/0363546512444554.
Dockree, P. M., & Robertson, I. H. (2011). Electrophysiological markers of cognitive deficits in traumatic brain injury: a review. International Journal of Psychophysiology, 82(1), 53–60. doi:10.1016/j.ijpsycho.2011.01.004.
Elbin, R. J., Schatz, P., & Covassin, T. (2011). One-year test-retest reliability of the online version of ImPACT in high school athletes. American Journal of Sports Medicine, 39(11), 2319–2324. doi:10.1177/0363546511417173.
Engel, A. K., Fries, P., & Singer, W. (2001). Dynamic predictions: oscillations and synchrony in top-down processing. Nature Reviews Neuroscience, 2(10), 704–716. doi:10.1038/35094565.
Erickson, J. C. (2011). Treatment outcomes of chronic post-traumatic headaches after mild head trauma in US soldiers: an observational study. Headache, 51(6), 932–944. doi:10.1111/j.1526-4610.2011.01909.x.
Field, M., Collins, M. W., Lovell, M. R., & Maroon, J. (2003). Does age play a role in recovery from sports-related concussion? a comparison of high school and collegiate athletes. Journal of Pediatrics, 142(5), 546–553. doi:10.1067/mpd.2003.190.
Fisher, T., Aharon-Peretz, J., & Pratt, H. (2011). Dis-regulation of response inhibition in adult attention deficit hyperactivity disorder (ADHD): an ERP study. Clinical Neurophysiology, 122(12), 2390–2399. doi:10.1016/j.clinph.2011.05.010.
Fries, P. (2005). A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends in Cognitive Science, 9(10), 474–480. doi:10.1016/j.tics.2005.08.011.
Giza, C. C., & Hovda, D. A. (2001). The neurometabolic cascade of concussion. Journal of Athletic Training, 36(3), 228–235.
Giza, C. C., & Hovda, D. A. (2014). The new neurometabolic cascade of concussion. Neurosurgery, 75(Suppl 4), S24–33. doi:10.1227/NEU.0000000000000505.
Gosselin, N., Bottari, C., Chen, J. K., Huntgeburth, S. C., De Beaumont, L., Petrides, M., et al. (2012). Evaluating the cognitive consequences of mild traumatic brain injury and concussion by using electrophysiology. Neurosurgical Focus, 33(6), 1–7. doi:10.3171/2012.10.FOCUS12253. E7.
Guskiewicz, K. M., Marshall, S. W., Bailes, J., McCrea, M., Harding, H. P., Jr., Matthews, A., et al. (2007). Recurrent concussion and risk of depression in retired professional football players. Medicine and Science in Sports and Exercise, 39(6), 903–909. doi:10.1249/mss.0b013e3180383da5.
Headache Classification Subcommittee of the International Headache, S. (2004). The international classification of headache disorders: 2nd edition. Cephalalgia, 24(Suppl 1), 9–160.
Iverson, G. L., Lovell, M. R., & Collins, M. W. (2003). Interpreting change on ImPACT following sport concussion. Clinical Neuropsychologist, 17(4), 460–467. doi:10.1076/clin.17.4.460.27934.
Kawamata, M., Kirino, E., Inoue, R., & Arai, H. (2007). Event-related desynchronization of frontal-midline theta rhythm during preconscious auditory oddball processing. Clinical EEG and Neuroscience, 38(4), 193–202.
Kontos, A. P., Elbin, R. J., Lau, B., Simensky, S., Freund, B., French, J., et al. (2013). Posttraumatic migraine as a predictor of recovery and cognitive impairment after sport-related concussion. American Journal of Sports Medicine, 41(7), 1497–1504. doi:10.1177/0363546513488751.
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.
Lau, B. C., Lovell, M. R., Collins, M. W., & Pardini, J. (2009). Neurocognitive and symptom predictors of recovery in high school athletes. Clinical Journal of Sport Medicine, 19(3), 216–221. doi:10.1097/JSM.0b013e31819d6edb.
Lau, B. C., Kontos, A. P., Collins, M. W., Mucha, A., & Lovell, M. R. (2011). Which on-field signs/symptoms predict protracted recovery from sport-related concussion among high school football players? American Journal of Sports Medicine, 39(11), 2311–2318. doi:10.1177/0363546511410655.
Lavoie, M. E., Dupuis, F., Johnston, K. M., Leclerc, S., & Lassonde, M. (2004). Visual p300 effects beyond symptoms in concussed college athletes. Journal of Clinical and Experimental Neuropsychology, 26(1), 55–73. doi:10.1076/jcen.26.1.55.23936.
Linden, R. D., Picton, T. W., Hamel, G., & Campbell, K. B. (1987). Human auditory steady-state evoked potentials during selective attention. Electroencephalography and Clinical Neurophysiology, 66(2), 145–159.
Lucas, S. (2011). Headache management in concussion and mild traumatic brain injury. Physical Medicine and Rehabilitation, 3(10 Suppl 2), S406–412. doi:10.1016/j.pmrj.2011.07.016.
McCrory, P., Meeuwisse, W. H., Aubry, M., Cantu, B., Dvorak, 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. Journal of the American College of Surgeons, 216(5), e55–71. doi:10.1016/j.jamcollsurg.2013.02.020.
Mihalik, J. P., Stump, J. E., Collins, M. W., Lovell, M. R., Field, M., & Maroon, J. C. (2005). Posttraumatic migraine characteristics in athletes following sports-related concussion. Journal of Neurosurgery, 102(5), 850–855. doi:10.3171/jns.2005.102.5.0850.
Mihalik, J. P., Register-Mihalik, J., Kerr, Z. Y., Marshall, S. W., McCrea, M. C., & Guskiewicz, K. M. (2013). Recovery of posttraumatic migraine characteristics in patients after mild traumatic brain injury. American Journal of Sports Medicine, 41(7), 1490–1496. doi:10.1177/0363546513487982.
Morlet, D., Demarquay, G., Brudon, F., Fischer, C., & Caclin, A. (2014). Attention orienting dysfunction with preserved automatic auditory change detection in migraine. Clinical Neurophysiology, 125(3), 500–511. doi:10.1016/j.clinph.2013.05.032.
Reches, A., Laufer, I., Ziv, K., Cukierman, G., McEvoy, K., Ettinger, M., et al. (2013). Network dynamics predict improvement in working memory performance following donepezil administration in healthy young adults. NeuroImage, 88C, 228–241. doi:10.1016/j.neuroimage.2013.11.020.
Reches, A., Levy-Cooperman, N., Laufer, I., Shani-Hershkovitch, R., Ziv, K., Kerem, D., et al. (2014). Brain network activation (BNA) reveals scopolamine-induced impairment of visual working memory. Journal of Molecular Neuroscience, 54(1), 59–70. doi:10.1007/s12031-014-0250-6.
Shahaf, G., Reches, A., Pinchuk, N., Fisher, T., Ben Bashat, G., Kanter, A., et al. (2012). Introducing a novel approach of network oriented analysis of ERPs, demonstrated on adult attention deficit hyperactivity disorder. Clinical Neurophysiology, 123(8), 1568–1580. doi:10.1016/j.clinph.2011.12.010.
Simmonds, D. J., Pekar, J. J., & Mostofsky, S. H. (2008). Meta-analysis of Go/No-go tasks demonstrating that fMRI activation associated with response inhibition is task-dependent. Neuropsychologia, 46(1), 224–232. doi:10.1016/j.neuropsychologia.2007.07.015.
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. doi:10.1016/j.neuroimage.2011.01.024.
Sporns, O. (2014). Contributions and challenges for network models in cognitive neuroscience. Nature Neuroscience, 17(5), 652–660. doi:10.1038/nn.3690.
Theriault, M., De Beaumont, L., Gosselin, N., Filipinni, M., & Lassonde, M. (2009). Electrophysiological abnormalities in well functioning multiple concussed athletes. Brain Injury, 23(11), 899–906. doi:10.1080/02699050903283189.
Wang, W., & Schoenen, J. (1998). Interictal potentiation of passive “oddball” auditory event-related potentials in migraine. Cephalalgia, 18(5), 261–265. discussion 241.
Compliance with ethical standards
Funding
This study was funded by ElMindA, Ltd. through a research contract with the University of Pittsburgh.
Conflict of interest
Authors Reches, Dickman, Laufer, Geva, and Shacham are employed by ElMindA, Ltd. With regard to the study data, Drs. Reches, Dickman, Laufer, Geva, and Shacham were not involved in data collection, entry, or analysis; they were only involved in blinded data transformation using the BNA algorithm and data interpretation of the BNA and EEG-ERP findings. Author Collins owns a 10 % share in ImPACT Applications, Inc. With regard to the study data, Dr. Collins was not involved in data collection, entry or analysis; he was only involved in data interpretation. Authors Kontos, Elbin, and DeWolf declare no conflict of interest.
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
Informed consent was obtained from all individual participants included in the study.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kontos, A.P., Reches, A., Elbin, R.J. et al. Preliminary evidence of reduced brain network activation in patients with post-traumatic migraine following concussion. Brain Imaging and Behavior 10, 594–603 (2016). https://doi.org/10.1007/s11682-015-9412-6
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11682-015-9412-6