Headache Related Alterations of Visual Processing in Migraine Patients.

Visual evoked potentials; chronic migraine; episodic migraine; feedback; feedforward; spectral analysis; Adult; Brain Waves/physiology; Chronic Disease; Evoked Potentials, Visual/physiology; Feedback; Female; Humans; Male; Middle Aged; Migraine Disorders/physiopathology; Visual Cortex/physiopathology; Visual Perception/physiology; Young Adult; Brain Waves; Evoked Potentials, Visual; Migraine Disorders; Visual Cortex; Visual Perception; Neurology; Neurology (clinical); Anesthesiology and Pain Medicine

Abstract :

[en] Migraine is characterized by an increased sensitivity to visual stimuli that worsens during attacks. Recent evidence has shown that feedforward volleys carrying incoming visual information induce high-frequency (gamma) oscillations in the visual cortex, while feedback volleys arriving from higher order brain areas induce oscillatory activity at lower frequencies (theta/alpha/low beta). We investigated visually induced high (feedforward) and low (feedback) frequency activations in healthy subjects and various migraine patients. Visual evoked potentials from 20 healthy controls and 70 migraine patients (30 interictal and 20 ictal episodic migraineurs, 20 chronic migraineurs) were analyzed in the frequency domain. We compared power in the theta-alpha-low beta and gamma range between groups, and searched for correlations between the low-to-high frequency activity ratio and number of monthly headache and migraine days. Compared to healthy controls, interictal migraine patients had increased visually induced low frequency (feedback) activity. Conversely, ictal and chronic migraine patients showed an augmented gamma band (feedforward) power. The low-frequency-to-gamma (feedback/feedforward) activity ratio correlated negatively with monthly headache days and tended to do so with migraine days. Our findings show that visual processing is differentially altered depending on migraine cycle and type. Feedback control from higher order cortical areas predominates interictally in episodic migraine while migraine attacks and chronic migraine are associated with enhanced incoming afferent activity, confirming their similar electrophysiological profile. The presence of headache is associated with proportionally higher gamma (feedforward) activities. PERSPECTIVE: This study provides an insight into the pathophysiology of migraine headache from the perspective of cortical sensory processing dynamics. Patients with migraine present alterations in feedback and feedforward visual signaling that differ with the presence of headache.

Disciplines :

Neurology

Author, co-author :

Lisicki, Marco; Headache Research Unit, CHR Citadelle Hospital, CHU de Liège, University of Liège Belgium

D'Ostilio, Kevin; Headache Research Unit, CHR Citadelle Hospital, CHU de Liège, University of Liège Belgium

Coppola, Gianluca; IRCCS - Fondazione Bietti, Research Unit of Neurophysiology of Vision and Neurophthalmology, Rome, Italy

Nonis, Romain; Headache Research Unit, CHR Citadelle Hospital, CHU de Liège, University of Liège Belgium

Maertens de Noordhout, Alain ; Centre Hospitalier Universitaire de Liège - CHU > > Service de neurologie (CHR)

Parisi, Vincenzo; IRCCS - Fondazione Bietti, Research Unit of Neurophysiology of Vision and Neurophthalmology, Rome, Italy

Magis, Delphine ; Université de Liège - ULiège > Département des sciences cliniques

Schoenen, Jean ; Centre Hospitalier Universitaire de Liège - CHU > > Service de neurologie (CHR)

Language :

English

Title :

Headache Related Alterations of Visual Processing in Migraine Patients.

Publication date :

2020

Journal title :

Journal of Pain

ISSN :

1526-5900

eISSN :

1528-8447

Publisher :

Churchill Livingstone Inc., United States

Volume :

Issue :

5-6

Pages :

593 - 602

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://api.elsevier.com/content/article/PII:S1526590019308223?httpAccept=text/xml

Funding text :

Funding: This project was part of the EUROHEADPAIN project - FP7 no. 602633 and received support from the Fonds d'Investissements de Recherche Scientifique (FIRS) of the CHU de Liège. GC was supported by the G.B. Bietti Foundation and the Italian Ministry of Health and Fondazione Roma.

Available on ORBi :

since 13 December 2022

Statistics

Number of views

37 (1 by ULiège)

Number of downloads

53 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Áfra, J, Proietti Cecchini, A, Sándor, PS, Schoenen, J, Comparison of visual and auditory evoked cortical potentials in migraine patients between attacks. Clin Neurophysiol 111 (2000), 1124–1129 [Internet]Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=10825720.
Ambrosini, A, Coppola, G, Gérardy, PY, Pierelli, F, Schoenen, J, Intensity dependence of auditory evoked potentials during light interference in migraine. Neurosci Lett 492 (2011), 80–83.
Boulloche, N, Denuelle, M, Payoux, P, Fabre, N, Trotter, Y, Géraud, G, Photophobia in migraine: An interictal PET study of cortical hyperexcitability and its modulation by pain. J Neurol Neurosurg Psychiatry 81 (2010), 978–984.
Chang, PF, Arendt-Nielsen, L, Chen, ACN, Dynamic changes and spatial correlation of EEG activities during cold pressor test in man. Brain Res Bull 57 (2002), 667–675 [Internet][cited 2018 Jul 31]. Available from http://www.ncbi.nlm.nih.gov/pubmed/11927371.
Chang, PF, Arendt-Nielsen, L, Graven-Nielsen, T, Svensson, P, Chen, AC, Topographic effects of tonic cutaneous nociceptive stimulation on human electroencephalograph. Neurosci Lett 305 (2001), 49–52 [Internet][cited 2018 Jul 31]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11356305.
Chen, WT, Wang, SJ, Fuh, JL, Lin, CP, Ko, YC, Lin, YY, Persistent ictal-like visual cortical excitability in chronic migraine. Pain 152 (2011), 254–258 [Internet] International Association for the Study of Pain;Available from: http://dx.doi.org/10.1016/j.pain.2010.08.047.
Coppola, G, Ambrosini, A, Di Clemente, L, Magis, D, Fumal, A, Gérard, P, Pierelli, F, Schoenen, J, Interictal abnormalities of gamma band activity in visual evoked responses in migraine: An indication of thalamocortical dysrhythmia?. Cephalalgia 27 (2007), 1360–1367 [Internet][cited 2016 Apr 29]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17986271.
Coppola, G, Iacovelli, E, Bracaglia, M, Serrao, M, Di Lorenzo, C, Pierelli, F, Electrophysiological correlates of episodic migraine chronification: Evidence for thalamic involvement. J Headache Pain, 14, 2013, 76 [Internet]Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3844625&tool=pmcentrez&rendertype=abstract.
Coppola, G, Di Lorenzo, C, Schoenen, J, Pierelli, F, Habituation and sensitization in primary headaches. J Headache Pain, 14, 2013, 65 [Internet]Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3733593&tool=pmcentrez&rendertype=abstract.
Coppola, G, Parisi, V, Di Lorenzo, C, Serrao, M, Magis, D, Schoenen, J, Pierelli, F, Lateral inhibition in visual cortex of migraine patients between attacks. J Headache Pain, 14, 2013, 20 [Internet][cited 2016 Feb 23]. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3620512&tool=pmcentrez&rendertype=abstract.
Coppola, G, Di Renzo, A, Tinelli, E, Di Lorenzo, C, Di Lorenzo, G, Parisi, V, Serrao, M, Schoenen, J, Pierelli, F, Thalamo-cortical network activity during spontaneous migraine attacks. Neurology 87 (2016), 2154–2160 [Internet][cited 2018 Feb 5]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27742813.
Coppola, G, Vandenheede, M, Di Clemente, L, Ambrosini, A, Fumal, A, De Pasqua, V, Schoenen, J, Somatosensory evoked high-frequency oscillations reflecting thalamo-cortical activity are decreased in migraine patients between attacks. Brain 128 (2005), 98–103 [Internet]Available from: http://www.ncbi.nlm.nih.gov/pubmed/15563513.
Delorme, A, Makeig, S, EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134 (2004), 9–21 [Internet][cited 2017 Apr 26]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/15102499.
Engel, AK, Fries, P, Singer, W, Dynamic predictions: Oscillations and synchrony in top–down processing. Nat Rev Neurosci 2 (2001), 704–716.
Fries, P, A mechanism for cognitive dynamics: Neuronal communication through neuronal coherence. Trends Cogn Sci, 2005, 474-480.
Goadsby, PJ, Holland, PR, Martins-Oliveira, M, Hoffmann, J, Schankin, C, Akerman, S, Pathophysiology of Migraine: A Disorder of Sensory Processing. Physiol Rev 97 (2017), 553–622 [Internet][cited 2017 Jun 1]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28179394.
Gross, J, Schnitzler, A, Timmermann, L, Ploner, M, Gamma oscillations in human primary somatosensory cortex reflect pain perception. Fries, P, (eds.) PLoS Biol, 5, 2007, e133 [Internet][cited 2018 Jul 31]. Available from: http://dx.plos.org/10.1371/journal.pbio.0050133.
Hauck, M, Lorenz, J, Engel, AK, Attention to painful stimulation enhances gamma-band activity and synchronization in human sensorimotor cortex. J Neurosci 27 (2007), 9270–9277 [Internet]Society for Neuroscience;[cited 2018 Jul 31]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17728441.
Hauck, M, Schröder, S, Meyer-Hamme, G, Lorenz, J, Friedrichs, S, Nolte, G, Gerloff, C, Engel, AK, Acupuncture analgesia involves modulation of pain-induced gamma oscillations and cortical network connectivity. Sci Rep, 7, 2017, 16307 [Internet] Nature Publishing Group;[cited 2018 Mar 28]. Available from: http://www.nature.com/articles/s41598-017-13633-4.
Headache Classification Committee of the International Headache Society (IHS). The International Classification of Headache Disorders, 3rd edition (beta version). Cephalalgia 53 (2013), 137–146 [Internet][cited 2016 Jul 28]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23771276.
Herrmann, CS, Munk, MHJ, Engel, AK, Cognitive functions of gamma-band activity: Memory match and utilization. Trends Cogn. Sci, 2004, 347–355.
Jensen, O, Bonnefond, M, VanRullen, R, An oscillatory mechanism for prioritizing salient unattended stimuli. Trends Cogn Sci Elsevier Current Trends, 2012, 200–205 [Internet][cited 2017 Nov 24]. Available from http://www.sciencedirect.com/science/article/pii/S1364661312000575.
Judit, A, Sándor, 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 20 (2000), 714–719 [Internet][cited 2016 Sep 20]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11167900.
van Kerkoerle, T, Self, MW, Dagnino, B, Gariel-Mathis, M-A, Poort, J, van der Togt, C, Roelfsema, PR, Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex. Proc Natl Acad Sci USA 111 (2014), 14332–14341 [Internet] National Academy of Sciences;[cited 2017 Nov 22]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25205811.
Lambert, GA, Hoskin, KL, Zagami, AS, Cortico-NRM influences on trigeminal neuronal sensation. Cephalalgia 28 (2008), 640–652.
Lipton, R, Cady, R, Stewart, W, Wilks, K, Hall, C, Diagnostic lessons from the spectrum study. Headache J Head Face Pain, 43, 2003, 423 [Internet] Wiley/Blackwell (10.1111)[cited 2018 Apr 4]. Available from: http://doi.wiley.com/10.1046/j.1526-4610.2003.03085_1.x.
Lisicki, M, D'Ostilio, K, Coppola, G, de Noordhout, AM, Parisi, V, Schoenen, J, Magis, D, Brain correlates of single trial visual evoked potentials in migraine: More than meets the eye. Front Neurol [Internet], 9, 2018, 393 Available from: https://www.frontiersin.org/article/10.3389/fneur.2018.00393/full.
Michalareas, G, Vezoli, J, van Pelt, S, Schoffelen, J-M, Kennedy, H, Fries, P, Alpha-Beta and Gamma Rhythms Subserve Feedback and Feedforward Influences among Human Visual Cortical Areas. Neuron 89 (2016), 384–397 [Internet][cited 2017 Nov 22]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26777277.
Muthukumaraswamy, SD, High-frequency brain activity and muscle artifacts in MEG/EEG: a review and recommendations. Front Hum Neurosci, 2013.
Nir, R-R, Sinai, A, Moont, R, Harari, E, Yarnitsky, D, Tonic pain and continuous EEG: Prediction of subjective pain perception by alpha-1 power during stimulation and at rest. Clin Neurophysiol 123 (2012), 605–612 [Internet][cited 2018 Jul 31]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21889398.
Noseda, R, Kainz, V, Jakubowski, M, Gooley, JJ, Saper, CB, Digre, K, Burstein, R, A neural mechanism for exacerbation of headache by light. Nat Neurosci 13 (2010), 239–245 [Internet] Nature Publishing Group;[cited 2016 May 29]. Available from: http://dx.doi.org/10.1038/nn.2475.
Peng, W, Hu, L, Zhang, Z, Hu, Y, Changes of spontaneous oscillatory activity to tonic heat pain. Zuo X-N, editor PLoS One, 9, 2014, e91052 [Internet] Public Library of Science;[cited 2018 Mar 28]. Available from: http://dx.plos.org/10.1371/journal.pone.0091052.
Pfurtscheller, G, Lopes da Silva, FH, Event-related EEG/MEG synchronization and desynchronization: Basic principles. Clin Neurophysiol 110 (1999), 1842–1857 [Internet][cited 2018 Aug 1]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10576479.
Porcaro, C, Di Lorenzo, G, Seri, S, Pierelli, F, Tecchio, F, Coppola, G, Impaired brainstem and thalamic high-frequency oscillatory EEG activity in migraine between attacks. Cephalalgia 37 (2017), 915–926.
Sakuma, K, Takeshima, T, Ishizaki, K, Nakashima, K, Somatosensory evoked high-frequency oscillations in migraine patients. Clin Neurophysiol 115 (2004), 1857–1862 [Internet][cited 2017 Sep 15]. Available from: http://www.clinph-journal.com/article/S1388-2457(04)00106-3/pdf.
Salinas, E, Sejnowski, TJ, Correlated neuronal activity and the flow of neural information. Nat Rev Neurosci, 2001, 539–550.
Sava, SL, De Pasqua, V, Magis, D, Schoenen, J, Effects of visual cortex activation on the nociceptive blink reflex in healthy subjects. PLoS One, 9, 2014, e100198.
Schoenen, J, Is chronic migraine a never-ending migraine attack?. Pain 152 (2011), 239–240 [Internet][cited 2016 Jan 24]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21168270.
Schulte, LH, May, A, The migraine generator revisited: Continuous scanning of the migraine cycle over 30 days and three spontaneous attacks. Brain 139 (2016), 1987–1993 [Internet][cited 2016 Aug 9]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27190019.
Siegel, M, Donner, TH, Oostenveld, R, Fries, P, Engel, AK, High-frequency activity in human visual cortex is modulated by visual motion strength. Cereb Cortex 17 (2007), 732–741.
Silberstein, SD, Dodick, DW, Bigal, ME, Yeung, PP, Goadsby, PJ, Blankenbiller, T, Grozinski-Wolff, M, Yang, R, Ma, Y, Aycardi, E, Fremanezumab for the Preventive Treatment of Chronic Migraine. N Engl J Med 377 (2017), 2113–2122 [Internet]Available from: http://www.nejm.org/doi/10.1056/NEJMoa1709038%0Ahttp://www.ncbi.nlm.nih.gov/pubmed/29171818.
Singer, W, Gray, C, Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18 (1995), 555–586 [Internet]Available from: http://www.ncbi.nlm.nih.gov/pubmed/7605074.
Siniatchkin, M, Reich, A-L, Shepherd, AJ, van Baalen, A, Siebner, HR, Stephani, U, Peri-ictal changes of cortical excitability in children suffering from migraine without aura. Pain 147 (2009), 132–140.
Tallon-Baudry, C, Bertrand, O, Oscillatory gamma activity and its role in object representation. Trends Cogn Sci 3 (1999), 151–162.
Tiemann, L, Schulz, E, Gross, J, Ploner, M, Gamma oscillations as a neuronal correlate of the attentional effects of pain. Pain 150 (2010), 302–308.
De Tommaso, M, Marinazzo, D, Guido, M, Libro, G, Stramaglia, S, Nitti, L, Lattanzi, G, Angelini, L, Pellicoro, M, Visually evoked phase synchronization changes of alpha rhythm in migraine: Correlations with clinical features. Int J Psychophysiol 57 (2005), 203–210.
Whitham, EM, Pope, KJ, Fitzgibbon, SP, Lewis, T, Clark, CR, Loveless, S, Broberg, M, Wallace, A, DeLosAngeles, D, Lillie, P, Hardy, A, Fronsko, R, Pulbrook, A, Willoughby, JO, Scalp electrical recording during paralysis: Quantitative evidence that EEG frequencies above 20 Hz are contaminated by EMG. Clin Neurophysiol 119 (2007), 1166–1175.
Yuval-Greenberg, S, Tomer, O, Keren, AS, Nelken, I, Deouell, LY, Transient induced Gamma-band response in EEG as a manifestation of miniature saccades. Neuron 58 (2008), 429–441.
Headache Classification Committee of the International Headache Society (IHS). The International Classification of Headache Disorders, 3rd edition, 38, 2018, Cephalalgia [Internet] SAGE PublicationsSage UK, London, England, 1–211 [cited 2018 Jan 27]. Available from: http://journals.sagepub.com/doi/10.1177/0333102417738202.