Effects of light deprivation on visual evoked potentials in migraine without aura.

Adult; Darkness; Evoked Potentials, Visual/physiology; Female; Habituation, Psychophysiologic/physiology; Humans; Male; Migraine Disorders/physiopathology; Visual Cortex/physiopathology

Abstract :

[en] BACKGROUND: The mechanisms underlying the interictal habituation deficit of cortical visual evoked potentials (VEP) in migraine are not well understood. Abnormal long-term functional plasticity of the visual cortex may play a role and it can be assessed experimentally by light deprivation (LD). METHODS: We have compared the effects of LD on VEP in migraine patients without aura between attacks (MO, n = 17) and in healthy volunteers (HV, n = 17). Six sequential blocks of 100 averaged VEP at 3.1 Hz were recorded before and after 1 hour of LD. We measured VEP P100 amplitude of the 1st block of 100 sweeps and its change over 5 sequential blocks of 100 responses. RESULTS: In HV, the consequence of LD was a reduction of 1st block VEP amplitude and of the normal habituation pattern. By contrast, in MO patients, the interictal habituation deficit was not significantly modified, although 1st block VEP amplitude, already lower than in HV before LD, further decreased after LD. CONCLUSIONS: Light deprivation is thought to decrease both excitatory and subsequent inhibitory processes in visual cortex, which is in line with our findings in healthy volunteers. The VEP results in migraine patients suggest that early excitation was adequately suppressed, but not the inhibitory mechanisms occurring during long term stimulation and habituation. Accordingly, deficient intracortical inhibition is unlikely to be a primary factor in migraine pathophysiology and the habituation deficit.

Disciplines :

Neurology

Author, co-author :

Coppola, Gianluca

Cremers, Julien ; Université de Liège - ULiège > Département des sciences cliniques > Neurologie

GERARD, Pascale ; Centre Hospitalier Universitaire de Liège - CHU > Neurologie CHR

Pierelli, Francesco

Schoenen, Jean ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Neuro-anatomie

Language :

English

Title :

Effects of light deprivation on visual evoked potentials in migraine without aura.

Publication date :

2011

Journal title :

BMC Neurology

eISSN :

1471-2377

Publisher :

BioMed Central

Volume :

Pages :

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 27 July 2012

Statistics

Number of views

114 (8 by ULiège)

Number of downloads

126 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Schoenen J, Wang W, Albert A, Delwaide P. Potentiation instead of habituation characterizes visual evoked potentials in migraine patients between attacks. Eur J Neurol 1995, 2:115-122.
Schoenen J. Deficient habituation of evoked cortical potentials in migraine: a link between brain biology, behavior and trigeminovascular activation?. Biomed Pharmacother 1996, 50(2):71-78. 10.1016/0753-3322(96)84716-0, 8761712.
Coppola G, Pierelli F, Schoenen J. Habituation and migraine. Neurobiol Learn Mem 2009, 92(2):249-259. 10.1016/j.nlm.2008.07.006, 18675928.
Mulleners WM, Chronicle EP, Palmer JE, Koehler PJ, Vredeveld JW. Visual cortex excitability in migraine with and without aura. Headache 2001, 41(6):565-572. 10.1046/j.1526-4610.2001.041006565.x, 11437892.
Brighina F, Palermo A, Fierro B. Cortical inhibition and habituation to evoked potentials: relevance for pathophysiology of migraine. J Headache Pain 2009, 10(2):77-84. 10.1007/s10194-008-0095-x, 19209386.
Thompson RF, Spencer WA. Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol Rev 1966, 73(1):16-43.
Rankin CH, Abrams T, Barry RJ, Bhatnagar S, Clayton DF, Colombo J, Coppola G, Geyer MA, Glanzman DL, Marsland S, McSweeney FK, Wilson DA, Wu CF, Thompson RF. Habituation revisited: an updated and revised description of the behavioral characteristics of habituation. Neurobiol Learn Mem 2009, 92(2):135-138. 10.1016/j.nlm.2008.09.012, 2754195, 18854219.
Coppola G, Currà A, Serrao M, Di Lorenzo C, Gorini M, Porretta E, Alibardi A, Parisi V, Pierelli F. Lack of cold pressor test-induced effect on visual-evoked potentials in migraine. J Headache Pain 2010, 11(2):115-121. 10.1007/s10194-009-0177-4, 20012123.
Smith GB, Heynen AJ, Bear MF. Bidirectional synaptic mechanisms of ocular dominance plasticity in visual cortex. Philos Trans R Soc Lond B Biol Sci 2009, 364(1515):357-367. 10.1098/rstb.2008.0198, 2674473, 18977732.
Rittenhouse CD, Shouval HZ, Paradiso MA, Bear MF. Monocular deprivation induces homosynaptic long-term depression in visual cortex. Nature 1999, 397(6717):347-350. 10.1038/16922, 9950426.
Tian N, Copenhagen DR. Visual deprivation alters development of synaptic function in inner retina after eye opening. Neuron 2001, 32(3):439-449. 10.1016/S0896-6273(01)00470-6, 11709155.
Giovannelli A, Di Marco S, Maccarone R, Bisti S. Long-term dark rearing induces permanent reorganization in retinal circuitry. Biochem Biophys Res Commun 2008, 365(2):349-354. 10.1016/j.bbrc.2007.10.204, 17999915.
Duffy KR, Slusar JE. Monocular deprivation provokes alteration of the neuronal cytoskeleton in developing cat lateral geniculate nucleus. Vis Neurosci 2009, 26(3):319-328. 10.1017/S0952523809090130, 19519963.
Gonzalez MMC, Aston-Jones G. Light deprivation damages monoamine neurons and produces a depressive behavioral phenotype in rats. Proc Natl Acad Sci USA 2008, 105(12):4898-4903. 10.1073/pnas.0703615105, 2290795, 18347342.
Zubek JP, Welch G. Electroencephalographic changes after prolonged sensory and perceptual deprivation. Science 1963, 139:1209-1210. 10.1126/science.139.3560.1209, 14003996.
Marjerrison G, Keogh RP. Electroencephalographic changes during brief periods of perceptual deprivation. Percept Mot Skills 1967, 24(2):611-615.
Snyder A, Shapley R. Deficits in the visual evoked potentials of cats as a result of visual deprivation. Exp Brain Res 1979, 37(1):73-86. 10.1007/BF01474255, 488219.
Postnikova NN, Nachkebiia AI, Lordkipanidze SO. [Evoked potentials in cortical and subcortical structures of the visual system to photic and acoustic stimuli under conditions of early light deprivation]. Zh Vyssh Nerv Deiat Im I P Pavlova 1977, 27(1):169-176.
Zislina NN. [Effect of early deprivation of visual evoked potentials of rabbit cerebral cortex under conditions of dark and light adaptation]. Zh Vyssh Nerv Deiat Im I P Pavlova 1977, 27(1):161-168.
Glass JD, Crowder JV, Kennerdell JS, Merikangas JR. Visually evoked potentials from occipital and precentral cortex in visually deprived humans. Electroencephalogr Clin Neurophysiol 1977, 43(2):207-217. 10.1016/0013-4694(77)90128-6, 69531.
Grigor'eva LP, Zislina NN, Tolstova VA. [Plasticity of the visual system and learning]. Fiziol Cheloveka 1996, 22(1):55-62.
Boroojerdi B, Bushara KO, Corwell B, Immisch I, Battaglia F, Muellbacher W, Cohen LG. Enhanced excitability of the human visual cortex induced by short-term light deprivation. Cereb Cortex 2000, 10(5):529-534. 10.1093/cercor/10.5.529, 10847602.
Fierro B, Brighina F, Vitello G, Piazza A, Scalia S, Giglia G, Daniele O, Pascual-Leone A. Modulatory effects of low- and high-frequency repetitive transcranial magnetic stimulation on visual cortex of healthy subjects undergoing light deprivation. J Physiol 2005, 565(Pt 2):659-665. 1464536, 15760946.
Marjerrison G, Keogh RP. The neurophysiology of schizophrenia. Field dependency and electroencephalogram (EEG) responses to perceptual deprivation. J Nerv Ment Dis 1971, 152(6):390-395. 10.1097/00005053-197106000-00002, 5562592.
Koch SP, Koendgen S, Bourayou R, Steinbrink J, Obrig H. Individual alpha-frequency correlates with amplitude of visual evoked potential and hemodynamic response. Neuroimage 2008, 41(2):233-242. 10.1016/j.neuroimage.2008.02.018, 18395469.
Hughes SW, Crunelli V. Thalamic mechanisms of EEG alpha rhythms and their pathological implications. Neuroscientist 2005, 11(4):357-372. 10.1177/1073858405277450, 16061522.
Steriade M, Llinás RR. The functional states of the thalamus and the associated neuronal interplay. Physiol Rev 1988, 68(3):649-742.
Lopes da Silva F. Neural mechanisms underlying brain waves: from neural membranes to networks. Electroencephalogr Clin Neurophysiol 1991, 79(2):81-93. 10.1016/0013-4694(91)90044-5, 1713832.
Bremer F, Stoupel N. [Facilitation and inhibition of evoked cortical potentials during cerebral arousal]. Arch Int Physiol Biochim 1959, 67(2):240-275. 10.3109/13813455909074432, 13650758.
Armengol V, Lifschitz W, Palestini M. Inhibitory influences on primary and secondary cortical photic potentials originating in the lower brain stem. J Physiol 1961, 159:451-460. 1359544, 13862344.
Fuster JM, Docter RF. Variations of optic evoked potentials as a function of reticular activity in rabbits with chronically implanted electrodes. J Neurophysiol 1962, 25:324-336.
Yashiro K, Corlew R, Philpot BD. Visual deprivation modifies both presynaptic glutamate release and the composition of perisynaptic/extrasynaptic NMDA receptors in adult visual cortex. J Neurosci 2005, 25(50):11684-11692. 10.1523/JNEUROSCI.4362-05.2005, 16354927.
Goel A, Lee HK. Persistence of experience-induced homeostatic synaptic plasticity through adulthood in superficial layers of mouse visual cortex. J Neurosci 2007, 27(25):6692-6700. 10.1523/JNEUROSCI.5038-06.2007, 2601561, 17581956.
Kirkwood A, Rioult MC, Bear MF. Experience-dependent modification of synaptic plasticity in visual cortex. Nature 1996, 381(6582):526-528. 10.1038/381526a0, 8632826.
Kreczko A, Goel A, Song L, Lee HK. Visual deprivation decreases somatic GAD65 puncta number on layer 2/3 pyramidal neurons in mouse visual cortex. Neural Plast 2009, 2009:415135. 2686200, 19503840.
Boroojerdi B, Battaglia F, Muellbacher W, Cohen LG. Mechanisms underlying rapid experience-dependent plasticity in the human visual cortex. Proc Natl Acad Sci USA 2001, 98(25):14698-14701. 10.1073/pnas.251357198, 64744, 11734655.
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 2007, 27(12):1360-1367. 10.1111/j.1468-2982.2007.01466.x, 17986271.
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 2005, 128(Pt 1):98-103.
Panconesi A. Serotonin and migraine: a reconsideration of the central theory. J Headache Pain 2008, 9(5):267-276. 10.1007/s10194-008-0058-2, 18668197.
Llinás RR, Ribary U, Jeanmonod D, Kronberg E, Mitra PP. Thalamocortical dysrhythmia: A neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc Natl Acad Sci USA 1999, 96(26):15222-15227. 10.1073/pnas.96.26.15222, 24801, 10611366.
Walton KD, Dubois M, Llinás RR. Abnormal thalamocortical activity in patients with Complex Regional Pain Syndrome (CRPS) Type I. Pain 2010,
Bear MF, Cooper LN, Ebner FF. A physiological basis for a theory of synapse modification. Science 1987, 237(4810):42-48. 10.1126/science.3037696, 3037696.
Bienenstock E, Cooper L, Munro P. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 1982, 2(1):32-48.
Montero V. Amblyopia decreases activation of the corticogeniculate pathway and visual thalamic reticularis in attentive rats: a 'focal attention' hypothesis. Neuroscience 1999, 91(3):805-817. 10.1016/S0306-4522(98)00632-0, 10391464.