Skip to main content

Advertisement

SpringerLink
Log in

Preventive drugs restore visual evoked habituation and attention in migraineurs

  • Original Article
  • Published:
Acta Neurologica Belgica Aims and scope Submit manuscript

Abstract

Visual system pathway dysfunction has been postulated in migraineurs. We wanted to investigate if any difference exists interictally in visual attention and visual evoked habituation of frequently attacked migraineurs compared to the healthy control group. The effects of 3-month prophylactic migraine treatment on these parameters were also assessed. The migraineurs at headache-free interval (n = 52) and age, sex-matched healthy controls (n = 35) were compared by habituation response to 10 blocks of repetitive pattern-reversal visual stimuli (each block consisted 100 responses). The amplitude changes of 5th and 10th blocks were further compared with that of block 1 to assess the response of habituation (i.e., decrease) or potentiation (i.e., increase). The level of sustained visual attention was assessed by Cancellation test. Migraineurs were randomized to three different preventive treatments: propranolol 40 mg tid, flunarizine 5 mg bid, or topiramate 50 mg bid. After 3 months of preventive treatment, migraineurs data were compared with their baseline values. The groups did not differ by sex and age. In electrophysiological studies, the habituation ability observed in the healthy group was not observed in migraineurs. However, it was restored 3 months after preventive treatment. In migraineurs, compared to their baseline values, the distorted visual attention parameters also improved after treatment. All drugs were effective. The loss of habituation ability and low visual attention performance in migraineurs can be restored by migraine preventive treatment. This electrophysiological study accompanied by neuropsychological test may aid an objective and quantitative assessment tool for understanding migraine pathophysiology.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Robbins MS, Lipton RB (2010) The epidemiology of primary headache disorders. Semin Neurol 30:107–119

    Article  PubMed  Google Scholar 

  2. Headache Classification Committee of the International Headache Society (IHS) (2013) The international classification of headache disorders, 3rd edition (beta version). Cephalalgia 33:629–808

    Article  Google Scholar 

  3. Choi JY, Oh K, Kim BJ, Chung CS, Koh SB, Park KW (2009) Usefulness of a photophobia questionnaire in patients with migraine. Cephalalgia 29:953–959

    Article  PubMed  Google Scholar 

  4. Digre KB, Brennan KC (2012) Shedding light on photophobia. J Neuroophthalmol 32:68–81

    Article  PubMed  PubMed Central  Google Scholar 

  5. Chronicle EP, Mulleners WM (1996) Visual system dysfunction in migraine: a review of clinical and psychophysical findings. Cephalalgia 16:525–535

    Article  CAS  PubMed  Google Scholar 

  6. Kowacs PA, Utiumi MA, Piovesan EJ (2015) The visual system in migraine: from the bench side to the office. Headache 55(Suppl 1):84–98

    Article  PubMed  Google Scholar 

  7. Martin H, del Rio MS, de Silanes CL, Alvarez-Linera J, Hernandez JA, Pareja JA (2011) Photoreactivity of the occipital cortex measured by functional magnetic resonance imaging-blood oxygenation level dependent in migraine patients and healthy volunteers: pathophysiological implications. Headache 51:1520–1528

    Article  PubMed  Google Scholar 

  8. Delange JM, Cutrer FM (2014) Our evolving understanding of migraine with aura. Curr Pain Headache Rep 18:453

    Article  PubMed  Google Scholar 

  9. Ambrosini A, Schoenen J (2003) The electrophysiology of migraine. Curr Opin Neurol 16:327–331

    Article  PubMed  Google Scholar 

  10. Sand T, Zhitniy N, White LR, Stovner LJ (2008) Visual evoked potential latency, amplitude and habituation in migraine: a longitudinal study. Clin Neurophysiol 119:1020–1027

    Article  PubMed  Google Scholar 

  11. Meyer JS, Thornby J, Crawford K, Rauch GM (2000) Reversible cognitive decline accompanies migraine and cluster headaches. Headache 40:638–646

    Article  CAS  PubMed  Google Scholar 

  12. Calandre EP, Bembibre J, Arnedo ML, Becerra D (2002) Cognitive disturbances and regional cerebral blood flow abnormalities in migraine patients: their relationship with the clinical manifestations of the illness. Cephalalgia 22:291–302

    Article  CAS  PubMed  Google Scholar 

  13. Suhr JA, Seng EK (2012) Neuropsychological functioning in migraine: clinical and research implications. Cephalalgia 32:39–54

    Article  PubMed  Google Scholar 

  14. Villa TR, Correa Moutran AR, Sobirai Diaz LA et al (2009) Visual attention in children with migraine: a controlled comparative study. Cephalalgia 29:631–634

    Article  CAS  PubMed  Google Scholar 

  15. Weintraub S, Mesulam MM (2000) Neuropsychological assessment of mental state. In: Mesulam MM (ed) Principles of behavioral and cognitive neurology. Oxford University Press, New York, pp 121–173

    Google Scholar 

  16. Headache Classification Subcommittee of the International Headache Society (2004) The international classification of headache disorders: 2nd edition. Cephalalgia 24(Suppl 1):1–160

    Google Scholar 

  17. Unal-Cevik I, Yildiz FG (2015) Visual snow in migraine with aura: further characterization by brain imaging, electrophysiology, and treatment-case report. Headache 55:1436–1441

    Article  PubMed  Google Scholar 

  18. Karakas S, Erdogan Bakar E, Dogutepe Dincer E (2006) Handbook of BILNOT battery: research and development of neuropsychological tests, 2nd edn. Eryilmaz Offset, Ankara

    Google Scholar 

  19. Stewart WF, Shechter A, Rasmussen BK (1994) Migraine prevalence. A review of population-based studies. Neurology 44:S17–S23

    CAS  PubMed  Google Scholar 

  20. Burstein R, Noseda R, Borsook D (2015) Migraine: multiple processes, complex pathophysiology. J Neurosci 35:6619–6629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Coppola G, Pierelli F, Schoenen J (2007) Is the cerebral cortex hyperexcitable or hyperresponsive in migraine? Cephalalgia 27:1427–1439

    Article  CAS  PubMed  Google Scholar 

  22. Coppola G, Ambrosini A, Di CL et al (2007) Interictal abnormalities of gamma band activity in visual evoked responses in migraine: an indication of thalamocortical dysrhythmia? Cephalalgia 27:1360–1367

    Article  CAS  PubMed  Google Scholar 

  23. De Tommaso M, Ambrosini A, Brighina F et al (2014) Altered processing of sensory stimuli in patients with migraine. Nat Rev Neurol 10:144–155

    Article  PubMed  Google Scholar 

  24. Hodkinson DJ, Wilcox SL, Veggeberg R et al (2016) increased amplitude of thalamocortical low-frequency oscillations in patients with migraine. J Neurosci 36:8026–8036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Schmitz N, Admiraal-Behloul F, Arkink EB et al (2008) Attack frequency and disease duration as indicators for brain damage in migraine. Headache 48:1044–1055

    Article  PubMed  Google Scholar 

  26. Terwindt GM, Ferrari MD, Tijhuis M, Groenen SM, Picavet HS, Launer LJ (2000) The impact of migraine on quality of life in the general population: the GEM study. Neurology 55:624–629

    Article  CAS  PubMed  Google Scholar 

  27. Mangun GR, Hillyard SA (1991) Modulations of sensory-evoked brain potentials indicate changes in perceptual processing during visual-spatial priming. J Exp Psychol Hum Percept Perform 17:1057–1074

    Article  CAS  PubMed  Google Scholar 

  28. Mickleborough MJ, Chapman CM, Toma AS, Chan JH, Truong G, Handy TC (2013) Interictal neurocognitive processing of visual stimuli in migraine: evidence from event-related potentials. PLoS One 8:e80920

    Article  PubMed  PubMed Central  Google Scholar 

  29. Annovazzi P, Colombo B, Bernasconi L, Schiatti E, Comi G, Leocani L (2004) Cortical function abnormalities in migraine: neurophysiological and neuropsychological evidence from reaction times and event-related potentials to the Stroop test. Neurol Sci 25(Suppl 3):S285–S287

    Article  PubMed  Google Scholar 

  30. Sukhodolsky DG, Leckman JF, Rothenberger A, Scahill L (2007) The role of abnormal neural oscillations in the pathophysiology of co-occurring Tourette syndrome and attention-deficit/hyperactivity disorder. Eur Child Adolesc Psychiatry 16(Suppl 1):51–59

    Article  PubMed  Google Scholar 

  31. Villa TR, Agessi LM, Moutran AR, Gabbai AA, Carvalho DS (2016) Visual attention in children with migraine: the importance of prophylaxis. J Child Neurol 31(5):569–572. doi:10.1177/0883073815601498

    Article  PubMed  Google Scholar 

  32. Mulleners WM, McCrory DC, Linde M (2015) Antiepileptics in migraine prophylaxis: an updated Cochrane review. Cephalalgia 35:51–62

    Article  PubMed  Google Scholar 

  33. Vecsei L, Majlath Z, Szok D, Csati A, Tajti J (2015) Drug safety and tolerability in prophylactic migraine treatment. Expert Opin Drug Saf 14:667–681

    Article  CAS  PubMed  Google Scholar 

  34. Thompson RF, Spencer WA (1966) Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol Rev 73:16–43

    Article  CAS  PubMed  Google Scholar 

  35. Sappey-Marinier D, Calabrese G, Fein G, Hugg JW, Biggins C, Weiner MW (1992) Effect of photic stimulation on human visual cortex lactate and phosphates using 1H and 31P magnetic resonance spectroscopy. J Cereb Blood Flow Metab 12:584–592

    Article  CAS  PubMed  Google Scholar 

  36. Schoenen J, Wang W, Albert A, Delwaide PJ (1995) Potentiation instead of habituation characterizes visual evoked potentials in migraine patients between attacks. Eur J Neurol 2:115–122

    Article  CAS  PubMed  Google Scholar 

  37. Omland PM, Uglem M, Hagen K, Linde M, Tronvik E, Sand T (2016) Visual evoked potentials in migraine: is the “neurophysiological hallmark” concept still valid? Clin Neurophysiol 127:810–816

    Article  PubMed  Google Scholar 

  38. Rauschel V, Ruscheweyh R, Krafczyk S, Straube A (2016) Test-retest reliability of visual-evoked potential habituation. Cephalalgia 36:831–839

    Article  PubMed  Google Scholar 

  39. Ambrosini A, Coppola G, Iezzi E, Pierelli F, Schoenen J (2016) Reliability and repeatability of testing visual evoked potential habituation in migraine: a blinded case-control study. Cephalalgia. doi:10.1177/0333102416648656

    Google Scholar 

  40. Gerwig M, Niehaus L, Stude P, Katsarava Z, Diener HC (2012) Beta-blocker migraine prophylaxis affects the excitability of the visual cortex as revealed by transcranial magnetic stimulation. J Headache Pain 13:83–89

    Article  CAS  PubMed  Google Scholar 

  41. Ye Q, Yan LY, Xue LJ et al (2011) Flunarizine blocks voltage-gated Na(+) and Ca(2+) currents in cultured rat cortical neurons: a possible locus of action in the prevention of migraine. Neurosci Lett 487:394–399

    Article  CAS  PubMed  Google Scholar 

  42. De Tommaso M, Guido M, Sardaro M et al (2008) Effects of topiramate and levetiracetam vs placebo on habituation of contingent negative variation in migraine patients. Neurosci Lett 442:81–85

    Article  PubMed  Google Scholar 

  43. Chen WT, Wang SJ, Fuh JL et al (2012) Visual cortex excitability and plasticity associated with remission from chronic to episodic migraine. Cephalalgia 32:537–543

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors report no conflict of interest and funding related with this manuscript.

Author information

Authors and Affiliations

  1. Department of Neurology, Ozel Ilke Yasam Medical Center, Dortyol, Turkey

    Ferda Ince

  2. Department of Psychology, Faculty of Science and Letter, Ufuk University, Ankara, Turkey

    Emel Erdogan-Bakar

  3. Department of Neurology, Faculty of Medicine, Pain Unit, Hacettepe University, Sıhhiye, 06100, Ankara, Turkey

    Isin Unal-Cevik

Authors
  1. Ferda Ince
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emel Erdogan-Bakar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Isin Unal-Cevik
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Isin Unal-Cevik.

Ethics declarations

Conflict of interest

Authors report no conflict of interest related with this manuscript.

Ethical Approval

The study was approved by the Local Ethical Commmitte.

Informed consent

Informed consent was obtained from participants.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ince, F., Erdogan-Bakar, E. & Unal-Cevik, I. Preventive drugs restore visual evoked habituation and attention in migraineurs. Acta Neurol Belg 117, 523–530 (2017). https://doi.org/10.1007/s13760-017-0749-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13760-017-0749-z

Keywords

Search

Navigation