Skip to main content

Advertisement

Log in

Migraine is Associated With Altered Processing of Sensory Stimuli

  • Migraine (R Cowan, Section Editor)
  • Published:
Current Pain and Headache Reports Aims and scope Submit manuscript

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.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

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

  1. The International Classification of Headache Disorders, 3rd edition (beta version). Cephalalgia. 2013;33:629-808.

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  9. Shibata K, Osawa M, Iwata M. Simultaneous recording of pattern reversal electroretinograms and visual evoked potentials in migraine. Cephalalgia. 1997;17:742–7.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Sprenger T, Borsook D. Migraine changes the brain: neuroimaging makes its mark. Curr Opin Neurol. 2012;25:252–62.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Cohen AS, Goadsby PJ. Functional neuroimaging of primary headache disorders. Curr Neurol Neurosci Rep. 2004;4:105–10.

    Article  PubMed  Google Scholar 

  16. Goadsby PJ. Neuroimaging in headache. Microsc Res Tech. 2001;53:179–87.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Vingen JV, Pareja JA, Storen O, White LR, Stovner LJ. Phonophobia in migraine. Cephalalgia. 1998;18:243–9.

    Article  PubMed  CAS  Google Scholar 

  19. Friedman DI, De ver Dye T. Migraine and the environment. Headache. 2009;49:941–52.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  24. Scharff L, Turk DC, Marcus DA. Triggers of headache episodes and coping responses of headache diagnostic groups. Headache. 1995;35:397–403.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  26. Snyder RD, Drummond PD. Olfaction in migraine. Cephalalgia. 1997;17:729–32.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  28. Stankewitz A, May A. Increased limbic and brainstem activity during migraine attacks following olfactory stimulation. Neurology. 2011;77:476–82.

    Article  PubMed  Google Scholar 

  29. Main A, Dowson A, Gross M. Photophobia and phonophobia in migraineurs between attacks. Headache. 1997;37:492–5.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  32. Noseda R, Kainz V, Jakubowski M, et al. A neural mechanism for exacerbation of headache by light. Nat Neurosci. 2010;13:239–45.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  34. Noseda R, Burstein R. Advances in understanding the mechanisms of migraine-type photophobia. Curr Opin Neurol. 2011;24:197–202.

    Article  PubMed  Google Scholar 

  35. Lipton RB, Bigal ME, Ashina S, et al. Cutaneous allodynia in the migraine population. Ann Neurol. 2008;63:148–58.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  37. Guven H, Cilliler AE, Comoglu SS. Cutaneous allodynia in patients with episodic migraine. Neurol Sci. 2013;34:1397–402.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Mesulam MM. From sensation to cognition. Brain. 1998;121(Pt 6):1013–52.

    Article  PubMed  Google Scholar 

  45. Stein BE, Stanford TR. Multisensory integration: current issues from the perspective of the single neuron. Nat Rev Neurosci. 2008;9:255–66.

    Article  PubMed  CAS  Google Scholar 

  46. Kelman L, Tanis D. The relationship between migraine pain and other associated symptoms. Cephalalgia. 2006;26:548–53.

    Article  PubMed  CAS  Google Scholar 

  47. Martin PR, Todd J, Reece J. Effects of noise and a stressor on head pain. Headache. 2005;45:1353–64.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Tyll S, Budinger E, Noesselt T. Thalamic influences on multisensory integration. Commun Integr Biol. 2011;4:378–81.

    PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  51. Coppola G, Di Lorenzo C, Schoenen J, Pierelli F. Habituation and sensitization in primary headaches. J Headache Pain. 2013;14:65.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Wang W, Schoenen J. Interictal potentiation of passive "oddball" auditory event-related potentials in migraine. Cephalalgia. 1998;18:261–5. discussion 241.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  54. Aurora SK, Wilkinson F. The brain is hyperexcitable in migraine. Cephalalgia. 2007;27:1442–53.

    Article  PubMed  CAS  Google Scholar 

  55. Drummond PD. Photophobia and autonomic responses to facial pain in migraine. Brain. 1997;120(Pt 10):1857–64.

    Article  PubMed  Google Scholar 

  56. Drummond PD, Woodhouse A. Painful stimulation of the forehead increases photophobia in migraine sufferers. Cephalalgia. 1993;13:321–4.

    Article  PubMed  CAS  Google Scholar 

  57. Oshinsky ML, Sanghvi MM, Maxwell CR, et al. Spontaneous trigeminal allodynia in rats: a model of primary headache. Headache. 2012;52:1336–49.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

  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.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

Download references

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

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Todd J. Schwedt.

Additional information

This article is part of the Topical Collection on Migraine

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Harriott, A.M., Schwedt, T.J. Migraine is Associated With Altered Processing of Sensory Stimuli. Curr Pain Headache Rep 18, 458 (2014). https://doi.org/10.1007/s11916-014-0458-8

Download citation

  • Published:

  • DOI: https://doi.org/10.1007/s11916-014-0458-8

Keywords

Navigation