Brain Imaging and Behavior

, Volume 10, Issue 2, pp 594–603 | Cite as

Preliminary evidence of reduced brain network activation in patients with post-traumatic migraine following concussion

  • Anthony P. Kontos
  • Amit Reches
  • R. J. Elbin
  • Dalia Dickman
  • Ilan Laufer
  • Amir B. Geva
  • Galit Shacham
  • Ryan DeWolf
  • Michael W. Collins
Original Research

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.

Keywords

Sport-related concussion Brain network activation Electroencephalography Post-traumatic migraine 

References

  1. 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.CrossRefPubMedGoogle Scholar
  2. 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.CrossRefPubMedGoogle Scholar
  3. 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.CrossRefPubMedGoogle Scholar
  4. 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.CrossRefPubMedGoogle Scholar
  5. 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.CrossRefPubMedGoogle Scholar
  6. Buzsaki, G., & Draguhn, A. (2004). Neuronal oscillations in cortical networks. Science, 304(5679), 1926–1929. doi:10.1126/science.1099745.CrossRefPubMedGoogle Scholar
  7. 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.CrossRefPubMedGoogle Scholar
  8. 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.CrossRefPubMedGoogle Scholar
  9. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 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.CrossRefPubMedGoogle Scholar
  12. 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.CrossRefPubMedGoogle Scholar
  13. 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.CrossRefPubMedGoogle Scholar
  14. 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.CrossRefPubMedGoogle Scholar
  15. 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.CrossRefPubMedGoogle Scholar
  16. 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.CrossRefPubMedGoogle Scholar
  17. 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.CrossRefPubMedGoogle Scholar
  18. 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.CrossRefGoogle Scholar
  19. Giza, C. C., & Hovda, D. A. (2001). The neurometabolic cascade of concussion. Journal of Athletic Training, 36(3), 228–235.PubMedPubMedCentralGoogle Scholar
  20. Giza, C. C., & Hovda, D. A. (2014). The new neurometabolic cascade of concussion. Neurosurgery, 75(Suppl 4), S24–33. doi:10.1227/NEU.0000000000000505.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. 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.CrossRefPubMedGoogle Scholar
  23. Headache Classification Subcommittee of the International Headache, S. (2004). The international classification of headache disorders: 2nd edition. Cephalalgia, 24(Suppl 1), 9–160.Google Scholar
  24. 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.CrossRefPubMedGoogle Scholar
  25. 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.CrossRefPubMedGoogle Scholar
  26. 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.CrossRefPubMedGoogle Scholar
  27. 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.CrossRefPubMedGoogle Scholar
  28. 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.CrossRefPubMedGoogle Scholar
  29. 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.CrossRefPubMedGoogle Scholar
  30. 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.CrossRefPubMedGoogle Scholar
  31. 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.CrossRefPubMedGoogle Scholar
  32. 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.Google Scholar
  33. 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.CrossRefPubMedGoogle Scholar
  34. 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.CrossRefPubMedGoogle Scholar
  35. 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.CrossRefPubMedGoogle Scholar
  36. 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.CrossRefPubMedGoogle Scholar
  37. 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.PubMedGoogle Scholar
  38. 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.CrossRefPubMedGoogle Scholar
  39. 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.CrossRefPubMedGoogle Scholar
  40. 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.CrossRefPubMedGoogle Scholar
  41. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Sporns, O. (2014). Contributions and challenges for network models in cognitive neuroscience. Nature Neuroscience, 17(5), 652–660. doi:10.1038/nn.3690.CrossRefPubMedGoogle Scholar
  43. 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.CrossRefPubMedGoogle Scholar
  44. Wang, W., & Schoenen, J. (1998). Interictal potentiation of passive “oddball” auditory event-related potentials in migraine. Cephalalgia, 18(5), 261–265. discussion 241.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Anthony P. Kontos
    • 1
  • Amit Reches
    • 2
  • R. J. Elbin
    • 3
  • Dalia Dickman
    • 2
  • Ilan Laufer
    • 2
  • Amir B. Geva
    • 2
  • Galit Shacham
    • 2
  • Ryan DeWolf
    • 1
  • Michael W. Collins
    • 1
  1. 1.Department of Orthopaedic Surgery/UPMC Sports Medicine Concussion ProgramUniversity of PittsburghPittsburghUSA
  2. 2.ElMindA, LtdTel AvivIsrael
  3. 3.Department of Health, Human Performance and Recreation/Office for Sport Concussion ResearchUniversity of ArkansasFayettevilleUSA

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