Advertisement

Migraine is Associated With Altered Processing of Sensory Stimuli

  • Andrea M. Harriott
  • Todd J. SchwedtEmail author
Migraine (R Cowan, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Migraine

Abstract

Migraine is associated with derangements in perception of multiple sensory modalities including vision, hearing, smell, and somatosensation. Compared to people without migraine, migraineurs have lower discomfort thresholds in response to special sensory stimuli as well as to mechanical and thermal noxious stimuli. Likewise, the environmental triggers of migraine attacks, such as odors and flashing lights, highlight basal abnormalities in sensory processing and integration. These alterations in sensory processing and perception in migraineurs have been investigated via physiological studies and functional brain imaging studies. Investigations have demonstrated that migraineurs during and between migraine attacks have atypical stimulus-induced activations of brainstem, subcortical, and cortical regions that participate in sensory processing. A lack of normal habituation to repetitive stimuli during the interictal state and a tendency towards development of sensitization likely contribute to migraine-related alterations in sensory processing.

Keywords

Migraine Sensory processing Migraine triggers Electrophysiology Functional neuroimaging 

Notes

Compliance with Ethics Guidelines

Conflict of Interest

Dr. Andrea M. Harriott declares no potential conflicts of interest.

Dr. Todd J. Schwedt reports grants from NIH K23NS070891, during the conduct of the study; personal fees from Allergan, personal fees from Zogenix, personal fees from Supernus, personal fees from Pfizer, grants from Merck.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Study Funding

NIH K23NS070891

References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. 1.
    The International Classification of Headache Disorders, 3rd edition (beta version). Cephalalgia. 2013;33:629-808.Google Scholar
  2. 2.
    de Tommaso M, Ambrosini A, Brighina F, et al. Altered processing of sensory stimuli in patients with migraine. Nat Rev Neurol. 2014;10:144–55.PubMedCrossRefGoogle Scholar
  3. 3.•
    Schwedt TJ. Multisensory integration in migraine. Curr Opin Neurol. 2013;26:248–53. This reference reviews the concept of and evidence for abnormal multisensory processing and integration in migraineurs.PubMedCrossRefPubMedCentralGoogle Scholar
  4. 4.
    Ambrosini A, de Noordhout AM, Sandor PS, Schoenen J. Electrophysiological studies in migraine: a comprehensive review of their interest and limitations. Cephalalgia. 2003;23 Suppl 1:13–31.PubMedCrossRefGoogle Scholar
  5. 5.
    Omland PM, Nilsen KB, Uglem M, et al. Visual evoked potentials in interictal migraine: no confirmation of abnormal habituation. Headache. 2013;53:1071–86.PubMedCrossRefGoogle Scholar
  6. 6.
    Logi F, Bonfiglio L, Orlandi G, Bonanni E, Iudice A, Sartucci F. Asymmetric scalp distribution of pattern visual evoked potentials during interictal phases in migraine. Acta Neurol Scand. 2001;104:301–7.PubMedCrossRefGoogle Scholar
  7. 7.
    Coppola G, Parisi V, Fiermonte G, Restuccia R, Pierelli F. Asymmetric distribution of visual evoked potentials in patients with migraine with aura during the interictal phase. Eur J Ophthalmol. 2007;17:828–35.PubMedGoogle Scholar
  8. 8.
    Afra J, Cecchini AP, De Pasqua V, Albert A, Schoenen J. Visual evoked potentials during long periods of pattern-reversal stimulation in migraine. Brain. 1998;121(Pt 2):233–41.PubMedCrossRefGoogle Scholar
  9. 9.
    Shibata K, Osawa M, Iwata M. Simultaneous recording of pattern reversal electroretinograms and visual evoked potentials in migraine. Cephalalgia. 1997;17:742–7.PubMedCrossRefGoogle Scholar
  10. 10.
    Sand T, Vingen JV. Visual, long-latency auditory and brainstem auditory evoked potentials in migraine: relation to pattern size, stimulus intensity, sound and light discomfort thresholds and pre-attack state. Cephalalgia. 2000;20:804–20.PubMedCrossRefGoogle Scholar
  11. 11.
    Coppola G, Vandenheede M, Di Clemente L, et al. Somatosensory evoked high-frequency oscillations reflecting thalamo-cortical activity are decreased in migraine patients between attacks. Brain. 2005;128:98–103.PubMedCrossRefGoogle Scholar
  12. 12.
    Judit A, Sandor PS, Schoenen J. Habituation of visual and intensity dependence of auditory evoked cortical potentials tends to normalize just before and during the migraine attack. Cephalalgia. 2000;20:714–9.PubMedCrossRefGoogle Scholar
  13. 13.
    Mickleborough MJ, Chapman CM, Toma AS, Chan JH, Truong G, Handy TC. Interictal neurocognitive processing of visual stimuli in migraine: evidence from event-related potentials. PLoS One. 2013;8:e80920.PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Sprenger T, Borsook D. Migraine changes the brain: neuroimaging makes its mark. Curr Opin Neurol. 2012;25:252–62.PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    Cohen AS, Goadsby PJ. Functional neuroimaging of primary headache disorders. Curr Neurol Neurosci Rep. 2004;4:105–10.PubMedCrossRefGoogle Scholar
  16. 16.
    Goadsby PJ. Neuroimaging in headache. Microsc Res Tech. 2001;53:179–87.PubMedCrossRefGoogle Scholar
  17. 17.
    Mainero C, Boshyan J, Hadjikhani N. Altered functional magnetic resonance imaging resting-state connectivity in periaqueductal gray networks in migraine. Ann Neurol. 2011;70:838–45.PubMedCrossRefPubMedCentralGoogle Scholar
  18. 18.
    Vingen JV, Pareja JA, Storen O, White LR, Stovner LJ. Phonophobia in migraine. Cephalalgia. 1998;18:243–9.PubMedCrossRefGoogle Scholar
  19. 19.
    Friedman DI, De ver Dye T. Migraine and the environment. Headache. 2009;49:941–52.PubMedCrossRefGoogle Scholar
  20. 20.•
    Noseda R, Burstein R. Migraine pathophysiology: anatomy of the trigeminovascular pathway and associated neurological symptoms, CSD, sensitization and modulation of pain. Pain. 2013;154 Suppl 1:S44–S53. This reference reviews the neuroanatomical and functional substrates for migraine pain and migraine related hypersensitivities to visual, auditory and olfactory stimuli.PubMedCrossRefGoogle Scholar
  21. 21.
    Noseda R, Jakubowski M, Kainz V, Borsook D, Burstein R. Cortical projections of functionally identified thalamic trigeminovascular neurons: implications for migraine headache and its associated symptoms. J Neurosci. 2011;31:14204–17.PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Chu CH, Liu CJ, Fuh JL, Shiao AS, Chen TJ, Wang SJ. Migraine is a risk factor for sudden sensorineural hearing loss: a nationwide population-based study. Cephalalgia. 2013;33:80–6.PubMedCrossRefGoogle Scholar
  23. 23.
    Bolay H, Bayazit YA, Gunduz B, et al. Subclinical dysfunction of cochlea and cochlear efferents in migraine: an otoacoustic emission study. Cephalalgia. 2008;28:309–17.PubMedCrossRefGoogle Scholar
  24. 24.
    Scharff L, Turk DC, Marcus DA. Triggers of headache episodes and coping responses of headache diagnostic groups. Headache. 1995;35:397–403.PubMedCrossRefGoogle Scholar
  25. 25.
    Kelman L. The place of osmophobia and taste abnormalities in migraine classification: a tertiary care study of 1237 patients. Cephalalgia. 2004;24:940–6.PubMedCrossRefGoogle Scholar
  26. 26.
    Snyder RD, Drummond PD. Olfaction in migraine. Cephalalgia. 1997;17:729–32.PubMedCrossRefGoogle Scholar
  27. 27.
    Demarquay G, Royet JP, Giraud P, Chazot G, Valade D, Ryvlin P. Rating of olfactory judgements in migraine patients. Cephalalgia. 2006;26:1123–30.PubMedCrossRefGoogle Scholar
  28. 28.
    Stankewitz A, May A. Increased limbic and brainstem activity during migraine attacks following olfactory stimulation. Neurology. 2011;77:476–82.PubMedCrossRefGoogle Scholar
  29. 29.
    Main A, Dowson A, Gross M. Photophobia and phonophobia in migraineurs between attacks. Headache. 1997;37:492–5.PubMedCrossRefGoogle Scholar
  30. 30.
    Vanagaite J, Pareja JA, Storen O, White LR, Sand T, Stovner LJ. Light-induced discomfort and pain in migraine. Cephalalgia. 1997;17:733–41.PubMedCrossRefGoogle Scholar
  31. 31.
    Kowacs PA, Piovesan EJ, Werneck LC, et al. Influence of intense light stimulation on trigeminal and cervical pain perception thresholds. Cephalalgia. 2001;21:184–8.PubMedCrossRefGoogle Scholar
  32. 32.
    Noseda R, Kainz V, Jakubowski M, et al. A neural mechanism for exacerbation of headache by light. Nat Neurosci. 2010;13:239–45.PubMedCrossRefPubMedCentralGoogle Scholar
  33. 33.
    Lovati C, Mariotti C, Giani L, et al. Central sensitization in photophobic and non-photophobic migraineurs: possible role of retino nuclear way in the central sensitization process. Neurol Sci. 2013;34 Suppl 1:S133–5.PubMedCrossRefGoogle Scholar
  34. 34.
    Noseda R, Burstein R. Advances in understanding the mechanisms of migraine-type photophobia. Curr Opin Neurol. 2011;24:197–202.PubMedCrossRefGoogle Scholar
  35. 35.
    Lipton RB, Bigal ME, Ashina S, et al. Cutaneous allodynia in the migraine population. Ann Neurol. 2008;63:148–58.PubMedCrossRefPubMedCentralGoogle Scholar
  36. 36.
    Bigal ME, Ashina S, Burstein R, et al. Prevalence and characteristics of allodynia in headache sufferers: a population study. Neurology. 2008;70:1525–33.PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    Guven H, Cilliler AE, Comoglu SS. Cutaneous allodynia in patients with episodic migraine. Neurol Sci. 2013;34:1397–402.PubMedCrossRefGoogle Scholar
  38. 38.
    Burstein R, Yarnitsky D, Goor-Aryeh I, Ransil BJ, Bajwa ZH. An association between migraine and cutaneous allodynia. Ann Neurol. 2000;47:614–24.PubMedCrossRefGoogle Scholar
  39. 39.
    Burstein R, Cutrer MF, Yarnitsky D. The development of cutaneous allodynia during a migraine attack clinical evidence for the sequential recruitment of spinal and supraspinal nociceptive neurons in migraine. Brain. 2000;123(Pt 8):1703–9.PubMedCrossRefGoogle Scholar
  40. 40.
    Burstein R, Collins B, Jakubowski M. Defeating migraine pain with triptans: a race against the development of cutaneous allodynia. Ann Neurol. 2004;55:19–26.PubMedCrossRefGoogle Scholar
  41. 41.
    Schwedt TJ, Krauss MJ, Frey K, Gereau RWT. Episodic and chronic migraineurs are hypersensitive to thermal stimuli between migraine attacks. Cephalalgia. 2011;31:6–12.PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Schwedt TJ, Larson-Prior L, Coalson RS, et al. Allodynia and descending pain modulation in migraine: a resting state functional connectivity analysis. Pain Med. 2014;15:154–65.PubMedCrossRefGoogle Scholar
  43. 43.
    Gierse-Plogmeier B, Colak-Ekici R, Wolowski A, Gralow I, Marziniak M, Evers S. Differences in trigeminal and peripheral electrical pain perception in women with and without migraine. J Headache Pain. 2009;10:249–54.PubMedCrossRefPubMedCentralGoogle Scholar
  44. 44.
    Mesulam MM. From sensation to cognition. Brain. 1998;121(Pt 6):1013–52.PubMedCrossRefGoogle Scholar
  45. 45.
    Stein BE, Stanford TR. Multisensory integration: current issues from the perspective of the single neuron. Nat Rev Neurosci. 2008;9:255–66.PubMedCrossRefGoogle Scholar
  46. 46.
    Kelman L, Tanis D. The relationship between migraine pain and other associated symptoms. Cephalalgia. 2006;26:548–53.PubMedCrossRefGoogle Scholar
  47. 47.
    Martin PR, Todd J, Reece J. Effects of noise and a stressor on head pain. Headache. 2005;45:1353–64.PubMedCrossRefGoogle Scholar
  48. 48.
    Ashkenazi A, Yang I, Mushtaq A, Oshinsky ML. Is phonophobia associated with cutaneous allodynia in migraine? J Neurol Neurosurg Psychiatry. 2010;81:1256–60.PubMedCrossRefPubMedCentralGoogle Scholar
  49. 49.
    Tyll S, Budinger E, Noesselt T. Thalamic influences on multisensory integration. Commun Integr Biol. 2011;4:378–81.PubMedPubMedCentralGoogle Scholar
  50. 50.
    Hoffken O, Stude P, Lenz M, Bach M, Dinse HR, Tegenthoff M. Visual paired-pulse stimulation reveals enhanced visual cortex excitability in migraineurs. Eur J Neurosci. 2009;30:714–20.PubMedCrossRefGoogle Scholar
  51. 51.
    Coppola G, Di Lorenzo C, Schoenen J, Pierelli F. Habituation and sensitization in primary headaches. J Headache Pain. 2013;14:65.PubMedCrossRefPubMedCentralGoogle Scholar
  52. 52.
    Wang W, Schoenen J. Interictal potentiation of passive "oddball" auditory event-related potentials in migraine. Cephalalgia. 1998;18:261–5. discussion 241.PubMedCrossRefGoogle Scholar
  53. 53.
    van der Kamp W, Maassen VanDenBrink A, Ferrari MD, van Dijk JG. Interictal cortical hyperexcitability in migraine patients demonstrated with transcranial magnetic stimulation. J Neurol Sci. 1996;139:106–10.PubMedCrossRefGoogle Scholar
  54. 54.
    Aurora SK, Wilkinson F. The brain is hyperexcitable in migraine. Cephalalgia. 2007;27:1442–53.PubMedCrossRefGoogle Scholar
  55. 55.
    Drummond PD. Photophobia and autonomic responses to facial pain in migraine. Brain. 1997;120(Pt 10):1857–64.PubMedCrossRefGoogle Scholar
  56. 56.
    Drummond PD, Woodhouse A. Painful stimulation of the forehead increases photophobia in migraine sufferers. Cephalalgia. 1993;13:321–4.PubMedCrossRefGoogle Scholar
  57. 57.
    Oshinsky ML, Sanghvi MM, Maxwell CR, et al. Spontaneous trigeminal allodynia in rats: a model of primary headache. Headache. 2012;52:1336–49.PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    Schwedt TJ, Schlaggar BL, Mar S, et al. Atypical resting-state functional connectivity of affective pain regions in chronic migraine. Headache. 2013;53:737–51.PubMedCrossRefPubMedCentralGoogle Scholar
  59. 59.
    Schwedt TJ, Chong CD, Chiang CC, Baxter L, Schlaggar BL, Dodick DW. Enhanced pain-induced activity of pain-processing regions in a case-control study of episodic migraine. Cephalalgia. 2014.Google Scholar
  60. 60.
    Moulton EA, Becerra L, Maleki N, et al. Painful heat reveals hyperexcitability of the temporal pole in interictal and ictal migraine States. Cereb Cortex. 2011;21:435–48.PubMedCrossRefPubMedCentralGoogle Scholar
  61. 61.
    Maleki N, Becerra L, Brawn J, Bigal M, Burstein R, Borsook D. Concurrent functional and structural cortical alterations in migraine. Cephalalgia. 2012;32:607–20.PubMedCrossRefGoogle Scholar
  62. 62.
    Russo A, Tessitore A, Esposito F, et al. Pain processing in patients with migraine: an event-related fMRI study during trigeminal nociceptive stimulation. J Neurol. 2012;259:1903–12.PubMedCrossRefGoogle Scholar
  63. 63.
    Moulton EA, Burstein R, Tully S, Hargreaves R, Becerra L, Borsook D. Interictal dysfunction of a brainstem descending modulatory center in migraine patients. PLoS One. 2008;3:e3799.PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    Kim JH, Kim S, Suh SI, Koh SB, Park KW, Oh K. Interictal metabolic changes in episodic migraine: a voxel-based FDG-PET study. Cephalalgia. 2010;30:53–61.PubMedGoogle Scholar
  65. 65.
    Boulloche N, Denuelle M, Payoux P, Fabre N, Trotter Y, Geraud G. Photophobia in migraine: an interictal PET study of cortical hyperexcitability and its modulation by pain. J Neurol Neurosurg Psychiatry. 2010;81:978–84.PubMedCrossRefGoogle Scholar
  66. 66.
    Demarquay G, Royet JP, Mick G, Ryvlin P. Olfactory hypersensitivity in migraineurs: a H(2)(15)O-PET study. Cephalalgia. 2008;28:1069–80.PubMedCrossRefGoogle Scholar
  67. 67.
    Liu J, Zhao L, Li G, et al. Hierarchical alteration of brain structural and functional networks in female migraine sufferers. PLoS One. 2012;7:e51250.PubMedCrossRefPubMedCentralGoogle Scholar
  68. 68.
    Zhao L, Liu J, Dong X, et al. Alterations in regional homogeneity assessed by fMRI in patients with migraine without aura stratified by disease duration. J Headache Pain. 2013;14:85.PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    Cao Y, Aurora SK, Nagesh V, Patel SC, Welch KM. Functional MRI-BOLD of brainstem structures during visually triggered migraine. Neurology. 2002;59:72–8.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Department of NeurologyMayo ClinicJacksonvilleUSA
  2. 2.Department of NeurologyMayo ClinicPhoenixUSA

Personalised recommendations