Skip to main content
Top
Published in: The Journal of Headache and Pain 6/2010

Open Access 01-12-2010 | Original

Changes in visual-evoked potential habituation induced by hyperventilation in migraine

Authors: Gianluca Coppola, Antonio Currà, Simona Liliana Sava, Alessia Alibardi, Vincenzo Parisi, Francesco Pierelli, Jean Schoenen

Published in: The Journal of Headache and Pain | Issue 6/2010

Login to get access

Abstract

Hyperventilation is often associated with stress, an established trigger factor for migraine. Between attacks, migraine is associated with a deficit in habituation to visual-evoked potentials (VEP) that worsens just before the attack. Hyperventilation slows electroencephalographic (EEG) activity and decreases the functional response in the occipital cortex during visual stimulation. The neural mechanisms underlying deficient-evoked potential habituation in migraineurs remain unclear. To find out whether hyperventilation alters VEP habituation, we recorded VEPs before and after experimentally induced hyperventilation lasting 3 min in 18 healthy subjects and 18 migraine patients between attacks. We measured VEP P100 amplitudes in six sequential blocks of 100 sweeps and habituation as the change in amplitude over the six blocks. In healthy subjects, hyperventilation decreased VEP amplitude in block 1 and abolished the normal VEP habituation. In migraine patients, hyperventilation further decreased the already low block 1 amplitude and worsened the interictal habituation deficit. Hyperventilation worsens the habituation deficit in migraineurs possibly by increasing dysrhythmia in the brainstem-thalamo-cortical network.
Literature
1.
go back to reference Amery WK, Vandenbergh V (1987) What can precipitating factors teach us about the pathogenesis of migraine? Headache 27:146–150, 1:STN:280:DyaL2s3kvFOntA%3D%3D, 10.1111/j.1526-4610.1987.hed2703146.x, 3597066CrossRefPubMed Amery WK, Vandenbergh V (1987) What can precipitating factors teach us about the pathogenesis of migraine? Headache 27:146–150, 1:STN:280:DyaL2s3kvFOntA%3D%3D, 10.1111/j.1526-4610.1987.hed2703146.x, 3597066CrossRefPubMed
2.
go back to reference Friedman SD, Jensen JE, Frederick BB, Artru AA, Renshaw PF et al (2007) Brain changes to hypocapnia using rapidly interleaved phosphorus-proton magnetic resonance spectroscopy at 4 T. J Cereb Blood Flow Metab 27:646–653, 1:CAS:528:DC%2BD2sXjtlKitbY%3D, 10.1038/sj.jcbfm.9600383, 16896347CrossRefPubMed Friedman SD, Jensen JE, Frederick BB, Artru AA, Renshaw PF et al (2007) Brain changes to hypocapnia using rapidly interleaved phosphorus-proton magnetic resonance spectroscopy at 4 T. J Cereb Blood Flow Metab 27:646–653, 1:CAS:528:DC%2BD2sXjtlKitbY%3D, 10.1038/sj.jcbfm.9600383, 16896347CrossRefPubMed
3.
go back to reference Friedman SD, Mathis CM, Hayes C, Renshaw P, Dager SR (2006) Brain pH response to hyperventilation in panic disorder: preliminary evidence for altered acid-base regulation. Am J Psychiatry 163:710–715, 10.1176/appi.ajp.163.4.710, 16585448CrossRefPubMed Friedman SD, Mathis CM, Hayes C, Renshaw P, Dager SR (2006) Brain pH response to hyperventilation in panic disorder: preliminary evidence for altered acid-base regulation. Am J Psychiatry 163:710–715, 10.1176/appi.ajp.163.4.710, 16585448CrossRefPubMed
4.
go back to reference van Rijen PC, Luyten PR, van der Sprenkel JW, Kraaier V, van Huffelen AC et al (1989) 1H and 31P NMR measurement of cerebral lactate, high-energy phosphate levels, and pH in humans during voluntary hyperventilation: associated EEG, capnographic, and Doppler findings. Magn Reson Med 10:182–193, 10.1002/mrm.1910100204, 2503671CrossRefPubMed van Rijen PC, Luyten PR, van der Sprenkel JW, Kraaier V, van Huffelen AC et al (1989) 1H and 31P NMR measurement of cerebral lactate, high-energy phosphate levels, and pH in humans during voluntary hyperventilation: associated EEG, capnographic, and Doppler findings. Magn Reson Med 10:182–193, 10.1002/mrm.1910100204, 2503671CrossRefPubMed
5.
go back to reference Jensen KE, Thomsen C, Henriksen O (1988) In vivo measurement of intracellular pH in human brain during different tensions of carbon dioxide in arterial blood. A 31P-NMR study. Acta Physiol Scand 134:295–298, 1:STN:280:DyaL1M7kslOkug%3D%3D, 10.1111/j.1748-1716.1988.tb08492.x, 3147578CrossRefPubMed Jensen KE, Thomsen C, Henriksen O (1988) In vivo measurement of intracellular pH in human brain during different tensions of carbon dioxide in arterial blood. A 31P-NMR study. Acta Physiol Scand 134:295–298, 1:STN:280:DyaL1M7kslOkug%3D%3D, 10.1111/j.1748-1716.1988.tb08492.x, 3147578CrossRefPubMed
6.
go back to reference Zwiener U, Löbel S, Rother M, Funke M (1998) Quantitative topographical analysis of EEG during nonstandardized and standardized hyperventilation. J Clin Neurophysiol 15:521–528, 1:STN:280:DyaK1M%2Fps1amsA%3D%3D, 10.1097/00004691-199811000-00011, 9881925CrossRefPubMed Zwiener U, Löbel S, Rother M, Funke M (1998) Quantitative topographical analysis of EEG during nonstandardized and standardized hyperventilation. J Clin Neurophysiol 15:521–528, 1:STN:280:DyaK1M%2Fps1amsA%3D%3D, 10.1097/00004691-199811000-00011, 9881925CrossRefPubMed
7.
go back to reference Matteo RS, Ornstein E, Schwartz AE, Young WL, Weinstein J et al (1992) Effects of hypocarbia on the pharmacodynamics of sufentanil in humans. Anesth Analg 75:186–192, 1:STN:280:DyaK38zjslWltA%3D%3D, 10.1213/00000539-199208000-00006, 1385931CrossRefPubMed Matteo RS, Ornstein E, Schwartz AE, Young WL, Weinstein J et al (1992) Effects of hypocarbia on the pharmacodynamics of sufentanil in humans. Anesth Analg 75:186–192, 1:STN:280:DyaK38zjslWltA%3D%3D, 10.1213/00000539-199208000-00006, 1385931CrossRefPubMed
8.
go back to reference Schubert A, Drummond JC (1986) The effect of acute hypocapnia on human median nerve somatosensory evoked responses. Anesth Analg 65:240–244, 1:STN:280:DyaL287ls1ylsg%3D%3D, 10.1213/00000539-198603000-00004, 3082246CrossRefPubMed Schubert A, Drummond JC (1986) The effect of acute hypocapnia on human median nerve somatosensory evoked responses. Anesth Analg 65:240–244, 1:STN:280:DyaL287ls1ylsg%3D%3D, 10.1213/00000539-198603000-00004, 3082246CrossRefPubMed
9.
go back to reference Huttunen J, Tolvanen H, Heinonen E, Voipio J, Wikström H et al (1999) Effects of voluntary hyperventilation on cortical sensory responses. Electroencephalographic and magnetoencephalographic studies. Exp Brain Res 125:248–254, 1:STN:280:DyaK1M3ksVShsw%3D%3D, 10.1007/s002210050680, 10229015CrossRefPubMed Huttunen J, Tolvanen H, Heinonen E, Voipio J, Wikström H et al (1999) Effects of voluntary hyperventilation on cortical sensory responses. Electroencephalographic and magnetoencephalographic studies. Exp Brain Res 125:248–254, 1:STN:280:DyaK1M3ksVShsw%3D%3D, 10.1007/s002210050680, 10229015CrossRefPubMed
10.
go back to reference Priori A, Berardelli A, Mercuri B, Inghilleri M, Manfredi M (1995) The effect of hyperventilation on motor cortical inhibition in humans: a study of the electromyographic silent period evoked by transcranial brain stimulation. Electroencephalogr Clin Neurophysiol 97:69–72, 1:STN:280:DyaK2M7ovVOrug%3D%3D, 10.1016/0924-980X(94)00224-U, 7533724CrossRefPubMed Priori A, Berardelli A, Mercuri B, Inghilleri M, Manfredi M (1995) The effect of hyperventilation on motor cortical inhibition in humans: a study of the electromyographic silent period evoked by transcranial brain stimulation. Electroencephalogr Clin Neurophysiol 97:69–72, 1:STN:280:DyaK2M7ovVOrug%3D%3D, 10.1016/0924-980X(94)00224-U, 7533724CrossRefPubMed
11.
go back to reference Sparing R, Dafotakis M, Buelte D, Meister IG, Noth J (2007) Excitability of human motor and visual cortex before, during, and after hyperventilation. J Appl Physiol 102:406–411, 10.1152/japplphysiol.00770.2006, 16990503CrossRefPubMed Sparing R, Dafotakis M, Buelte D, Meister IG, Noth J (2007) Excitability of human motor and visual cortex before, during, and after hyperventilation. J Appl Physiol 102:406–411, 10.1152/japplphysiol.00770.2006, 16990503CrossRefPubMed
12.
go back to reference Posse S, Kemna LJ, Elghahwagi B, Wiese S, Kiselev VG (2001) Effect of graded hypo- and hypercapnia on fMRI contrast in visual cortex: quantification of T(*)(2) changes by multiecho EPI. Magn Reson Med 46:264–271, 1:STN:280:DC%2BD3MvivFOkuw%3D%3D, 10.1002/mrm.1187, 11477629CrossRefPubMed Posse S, Kemna LJ, Elghahwagi B, Wiese S, Kiselev VG (2001) Effect of graded hypo- and hypercapnia on fMRI contrast in visual cortex: quantification of T(*)(2) changes by multiecho EPI. Magn Reson Med 46:264–271, 1:STN:280:DC%2BD3MvivFOkuw%3D%3D, 10.1002/mrm.1187, 11477629CrossRefPubMed
13.
go back to reference Weckesser M, Posse S, Olthoff U, Kemna L, Dager S et al (1999) Functional imaging of the visual cortex with bold-contrast MRI: hyperventilation decreases signal response. Magn Reson Med 41:213–216, 1:STN:280:DyaK1M7kvVGjsg%3D%3D, 10.1002/(SICI)1522-2594(199901)41:1<213::AID-MRM31>3.0.CO;2-S, 10025633CrossRefPubMed Weckesser M, Posse S, Olthoff U, Kemna L, Dager S et al (1999) Functional imaging of the visual cortex with bold-contrast MRI: hyperventilation decreases signal response. Magn Reson Med 41:213–216, 1:STN:280:DyaK1M7kvVGjsg%3D%3D, 10.1002/(SICI)1522-2594(199901)41:1<213::AID-MRM31>3.0.CO;2-S, 10025633CrossRefPubMed
14.
go back to reference Burykh EA (2008) Interaction of hypocapnia, hypoxia, brain blood flow, and brain electrical activity in voluntary hyperventilation in humans. Neurosci Behav Physiol 38:647–659, 1:STN:280:DC%2BD1crntFWgug%3D%3D, 10.1007/s11055-008-9029-y, 18709467CrossRefPubMed Burykh EA (2008) Interaction of hypocapnia, hypoxia, brain blood flow, and brain electrical activity in voluntary hyperventilation in humans. Neurosci Behav Physiol 38:647–659, 1:STN:280:DC%2BD1crntFWgug%3D%3D, 10.1007/s11055-008-9029-y, 18709467CrossRefPubMed
15.
go back to reference Kraaier V, van Huffelen AC, Wieneke GH (1988) Changes in quantitative EEG and blood flow velocity due to standardized hyperventilation; a model of transient ischaemia in young human subjects. Electroencephalogr Clin Neurophysiol 70:377–387, 1:STN:280:DyaL1M%2FjtVCkug%3D%3D, 10.1016/0013-4694(88)90015-6, 2460311CrossRefPubMed Kraaier V, van Huffelen AC, Wieneke GH (1988) Changes in quantitative EEG and blood flow velocity due to standardized hyperventilation; a model of transient ischaemia in young human subjects. Electroencephalogr Clin Neurophysiol 70:377–387, 1:STN:280:DyaL1M%2FjtVCkug%3D%3D, 10.1016/0013-4694(88)90015-6, 2460311CrossRefPubMed
16.
go back to reference Groves PM, Thompson RF (1970) Habituation: a dual-process theory. Psychol Rev 77:419–450, 1:STN:280:DyaE3M%2Fgt1Ohuw%3D%3D, 10.1037/h0029810, 4319167CrossRefPubMed Groves PM, Thompson RF (1970) Habituation: a dual-process theory. Psychol Rev 77:419–450, 1:STN:280:DyaE3M%2Fgt1Ohuw%3D%3D, 10.1037/h0029810, 4319167CrossRefPubMed
17.
go back to reference Sappey-Marinier D, Calabrese G, Fein G, Hugg JW, Biggins C et al (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, 1:CAS:528:DyaK38Xls1ynsL8%3D, 1618937CrossRefPubMed Sappey-Marinier D, Calabrese G, Fein G, Hugg JW, Biggins C et al (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, 1:CAS:528:DyaK38Xls1ynsL8%3D, 1618937CrossRefPubMed
18.
go back to reference Bohotin V, Fumal A, Vandenheede M, Gérard P, Bohotin C et al (2002) Effects of repetitive transcranial magnetic stimulation on visual evoked potentials in migraine. Brain 125:912–922, 1:STN:280:DC%2BD387nvFakuw%3D%3D, 10.1093/brain/awf081, 11912123CrossRefPubMed Bohotin V, Fumal A, Vandenheede M, Gérard P, Bohotin C et al (2002) Effects of repetitive transcranial magnetic stimulation on visual evoked potentials in migraine. Brain 125:912–922, 1:STN:280:DC%2BD387nvFakuw%3D%3D, 10.1093/brain/awf081, 11912123CrossRefPubMed
19.
go back to reference Coppola G, Serrao M, Currà A, Di Lorenzo C, Vatrika M et al (2010) Tonic pain abolishes cortical habituation of visual evoked potentials in healthy subjects. J Pain 11:291–296, 10.1016/j.jpain.2009.08.012, 20015701CrossRefPubMed Coppola G, Serrao M, Currà A, Di Lorenzo C, Vatrika M et al (2010) Tonic pain abolishes cortical habituation of visual evoked potentials in healthy subjects. J Pain 11:291–296, 10.1016/j.jpain.2009.08.012, 20015701CrossRefPubMed
20.
go back to reference Ozkul Y, Bozlar S (2002) Effects of fluoxetine on habituation of pattern reversal visually evoked potentials in migraine prophylaxis. Headache 42:582–587, 10.1046/j.1526-4610.2002.02144.x, 12482209CrossRefPubMed Ozkul Y, Bozlar S (2002) Effects of fluoxetine on habituation of pattern reversal visually evoked potentials in migraine prophylaxis. Headache 42:582–587, 10.1046/j.1526-4610.2002.02144.x, 12482209CrossRefPubMed
21.
go back to reference Schoenen J (1996) Deficient habituation of evoked cortical potentials in migraine: a link between brain biology, behavior and trigeminovascular activation? Biomed Pharmacother 50:71–78, 1:STN:280:DyaK28zhvFWntQ%3D%3D, 10.1016/0753-3322(96)84716-0, 8761712CrossRefPubMed Schoenen J (1996) Deficient habituation of evoked cortical potentials in migraine: a link between brain biology, behavior and trigeminovascular activation? Biomed Pharmacother 50:71–78, 1:STN:280:DyaK28zhvFWntQ%3D%3D, 10.1016/0753-3322(96)84716-0, 8761712CrossRefPubMed
22.
go back to reference Coppola G, Pierelli F, Schoenen J (2009) Habituation and migraine. Neurobiol Learn Mem 92:249–259, 10.1016/j.nlm.2008.07.006, 18675928CrossRefPubMed Coppola G, Pierelli F, Schoenen J (2009) Habituation and migraine. Neurobiol Learn Mem 92:249–259, 10.1016/j.nlm.2008.07.006, 18675928CrossRefPubMed
23.
go back to reference Coppola G, Currà A, Serrao M, Di Lorenzo C, Gorini M et al (2010) Lack of cold pressor test-induced effect on visual-evoked potentials in migraine. J Headache Pain 11:115–121, 10.1007/s10194-009-0177-4, 20012123PubMedCentralCrossRefPubMed Coppola G, Currà A, Serrao M, Di Lorenzo C, Gorini M et al (2010) Lack of cold pressor test-induced effect on visual-evoked potentials in migraine. J Headache Pain 11:115–121, 10.1007/s10194-009-0177-4, 20012123PubMedCentralCrossRefPubMed
24.
go back to reference Kraaier V, Van Huffelen AC, Wieneke GH, Van der Worp HB, Bär PR (1992) Quantitative EEG changes due to cerebral vasoconstriction. Indomethacin versus hyperventilation-induced reduction in cerebral blood flow in normal subjects. Electroencephalogr Clin Neurophysiol 82:208–212, 1:STN:280:DyaK387msVCrtQ%3D%3D, 10.1016/0013-4694(92)90169-I, 1371441CrossRefPubMed Kraaier V, Van Huffelen AC, Wieneke GH, Van der Worp HB, Bär PR (1992) Quantitative EEG changes due to cerebral vasoconstriction. Indomethacin versus hyperventilation-induced reduction in cerebral blood flow in normal subjects. Electroencephalogr Clin Neurophysiol 82:208–212, 1:STN:280:DyaK387msVCrtQ%3D%3D, 10.1016/0013-4694(92)90169-I, 1371441CrossRefPubMed
25.
go back to reference Hoshi Y, Okuhara H, Nakane S, Hayakawa K, Kobayashi N et al (1999) Re-evaluation of the hypoxia theory as the mechanism of hyperventilation-induced EEG slowing. Pediatr Neurol 21:638–643, 1:STN:280:DyaK1MvktFynuw%3D%3D, 10.1016/S0887-8994(99)00063-6, 10513691CrossRefPubMed Hoshi Y, Okuhara H, Nakane S, Hayakawa K, Kobayashi N et al (1999) Re-evaluation of the hypoxia theory as the mechanism of hyperventilation-induced EEG slowing. Pediatr Neurol 21:638–643, 1:STN:280:DyaK1MvktFynuw%3D%3D, 10.1016/S0887-8994(99)00063-6, 10513691CrossRefPubMed
26.
go back to reference Patel VM, Maulsby RL (1987) How hyperventilation alters the electroencephalogram: a review of controversial viewpoints emphasizing neurophysiological mechanisms. J Clin Neurophysiol 4:101–120, 1:STN:280:DyaL2szgvVOmuw%3D%3D, 10.1097/00004691-198704000-00001, 3305571CrossRefPubMed Patel VM, Maulsby RL (1987) How hyperventilation alters the electroencephalogram: a review of controversial viewpoints emphasizing neurophysiological mechanisms. J Clin Neurophysiol 4:101–120, 1:STN:280:DyaL2szgvVOmuw%3D%3D, 10.1097/00004691-198704000-00001, 3305571CrossRefPubMed
27.
go back to reference Koch SP, Koendgen S, Bourayou R, Steinbrink J, Obrig H (2008) Individual alpha-frequency correlates with amplitude of visual evoked potential and hemodynamic response. Neuroimage 41:233–242, 10.1016/j.neuroimage.2008.02.018, 18395469CrossRefPubMed Koch SP, Koendgen S, Bourayou R, Steinbrink J, Obrig H (2008) Individual alpha-frequency correlates with amplitude of visual evoked potential and hemodynamic response. Neuroimage 41:233–242, 10.1016/j.neuroimage.2008.02.018, 18395469CrossRefPubMed
28.
go back to reference Gavriysky VS (1991) Influence of a twofold voluntary hyperventilation on visually evoked cortical potentials and human pupillogram. Doc Ophthalmol 77:213–224, 1:STN:280:DyaK387gsVSlsQ%3D%3D, 10.1007/BF00161369, 1760970CrossRefPubMed Gavriysky VS (1991) Influence of a twofold voluntary hyperventilation on visually evoked cortical potentials and human pupillogram. Doc Ophthalmol 77:213–224, 1:STN:280:DyaK387gsVSlsQ%3D%3D, 10.1007/BF00161369, 1760970CrossRefPubMed
29.
go back to reference Davies HD, Carroll WM, Mastaglia FL (1986) Effects of hyperventilation on pattern-reversal visual evoked potentials in patients with demyelination. J Neurol Neurosurg Psychiatry 49:1392–1396, 1:STN:280:DyaL2s7htFKisQ%3D%3D, 10.1136/jnnp.49.12.1392, 3806116PubMedCentralCrossRefPubMed Davies HD, Carroll WM, Mastaglia FL (1986) Effects of hyperventilation on pattern-reversal visual evoked potentials in patients with demyelination. J Neurol Neurosurg Psychiatry 49:1392–1396, 1:STN:280:DyaL2s7htFKisQ%3D%3D, 10.1136/jnnp.49.12.1392, 3806116PubMedCentralCrossRefPubMed
30.
go back to reference Steriade M, Llinás RR (1988) The functional states of the thalamus and the associated neuronal interplay. Physiol Rev 68:649–742, 1:STN:280:DyaL1c3nslSqtQ%3D%3D, 2839857PubMed Steriade M, Llinás RR (1988) The functional states of the thalamus and the associated neuronal interplay. Physiol Rev 68:649–742, 1:STN:280:DyaL1c3nslSqtQ%3D%3D, 2839857PubMed
31.
go back to reference Lopes da Silva F (1991) Neural mechanisms underlying brain waves: from neural membranes to networks. Electroencephalogr Clin Neurophysiol 79:81–93, 1:STN:280:DyaK3MzitlaksQ%3D%3D, 10.1016/0013-4694(91)90044-5, 1713832CrossRefPubMed Lopes da Silva F (1991) Neural mechanisms underlying brain waves: from neural membranes to networks. Electroencephalogr Clin Neurophysiol 79:81–93, 1:STN:280:DyaK3MzitlaksQ%3D%3D, 10.1016/0013-4694(91)90044-5, 1713832CrossRefPubMed
32.
go back to reference Sherwin I (1965) Differential effects of hyperventilation on the excitability of intact and isolated cortex. Electroencephalogr Clin Neurophysiol 18:599–607, 1:STN:280:DyaF2M7gtFCntw%3D%3D, 10.1016/0013-4694(65)90077-5, 14296837CrossRefPubMed Sherwin I (1965) Differential effects of hyperventilation on the excitability of intact and isolated cortex. Electroencephalogr Clin Neurophysiol 18:599–607, 1:STN:280:DyaF2M7gtFCntw%3D%3D, 10.1016/0013-4694(65)90077-5, 14296837CrossRefPubMed
33.
go back to reference Sherwin I (1967) Alterations in the non-specific cortical afference during hyperventilation. Electroencephalogr Clin Neurophysiol 23:532–538, 1:STN:280:DyaF1c7isVaksQ%3D%3D, 10.1016/0013-4694(67)90019-3, 4169823CrossRefPubMed Sherwin I (1967) Alterations in the non-specific cortical afference during hyperventilation. Electroencephalogr Clin Neurophysiol 23:532–538, 1:STN:280:DyaF1c7isVaksQ%3D%3D, 10.1016/0013-4694(67)90019-3, 4169823CrossRefPubMed
34.
go back to reference Bonvallet M, Dell P, Hiebel G (1954) Sympathetic tonus and cortical electrical activity. Electroencephalogr Clin Neurophysiol 6:119–144, 1:STN:280:DyaG2c%2FmtFygtw%3D%3D, 10.1016/0013-4694(54)90011-5, 13141926CrossRefPubMed Bonvallet M, Dell P, Hiebel G (1954) Sympathetic tonus and cortical electrical activity. Electroencephalogr Clin Neurophysiol 6:119–144, 1:STN:280:DyaG2c%2FmtFygtw%3D%3D, 10.1016/0013-4694(54)90011-5, 13141926CrossRefPubMed
35.
go back to reference Bonvallet M, Dell P (1956) Somatic functions of the nervous system. Annu Rev Physiol 18:309–338, 1:STN:280:DyaG2s%2FgtFaguw%3D%3D, 10.1146/annurev.ph.18.030156.001521, 13355220CrossRefPubMed Bonvallet M, Dell P (1956) Somatic functions of the nervous system. Annu Rev Physiol 18:309–338, 1:STN:280:DyaG2s%2FgtFaguw%3D%3D, 10.1146/annurev.ph.18.030156.001521, 13355220CrossRefPubMed
36.
go back to reference Munk MH, Roelfsema PR, König P, Engel AK, Singer W (1996) Role of reticular activation in the modulation of intracortical synchronization. Science 272:271–274, 1:CAS:528:DyaK28Xit1KqsLo%3D, 10.1126/science.272.5259.271, 8602512CrossRefPubMed Munk MH, Roelfsema PR, König P, Engel AK, Singer W (1996) Role of reticular activation in the modulation of intracortical synchronization. Science 272:271–274, 1:CAS:528:DyaK28Xit1KqsLo%3D, 10.1126/science.272.5259.271, 8602512CrossRefPubMed
37.
go back to reference Destexhe A, Sejnowski TJ (2003) Interactions between membrane conductances underlying thalamocortical slow-wave oscillations. Physiol Rev 83:1401–1453, 1:CAS:528:DC%2BD3sXoslyjtrs%3D, 14506309PubMedCentralCrossRefPubMed Destexhe A, Sejnowski TJ (2003) Interactions between membrane conductances underlying thalamocortical slow-wave oscillations. Physiol Rev 83:1401–1453, 1:CAS:528:DC%2BD3sXoslyjtrs%3D, 14506309PubMedCentralCrossRefPubMed
38.
go back to reference Chesler M, Kaila K (1992) Modulation of pH by neuronal activity. Trends Neurosci 15:396–402, 1:CAS:528:DyaK3sXls1Ogtg%3D%3D, 10.1016/0166-2236(92)90191-A, 1279865CrossRefPubMed Chesler M, Kaila K (1992) Modulation of pH by neuronal activity. Trends Neurosci 15:396–402, 1:CAS:528:DyaK3sXls1Ogtg%3D%3D, 10.1016/0166-2236(92)90191-A, 1279865CrossRefPubMed
39.
go back to reference Mäkiranta MJ, Ruohonen J, Suominen K, Sonkajärvi E, Salomäki T et al (2004) BOLD-contrast functional MRI signal changes related to intermittent rhythmic delta activity in EEG during voluntary hyperventilation-simultaneous EEG and fMRI study. Neuroimage 22:222–231, 10.1016/j.neuroimage.2004.01.004, 15110012CrossRefPubMed Mäkiranta MJ, Ruohonen J, Suominen K, Sonkajärvi E, Salomäki T et al (2004) BOLD-contrast functional MRI signal changes related to intermittent rhythmic delta activity in EEG during voluntary hyperventilation-simultaneous EEG and fMRI study. Neuroimage 22:222–231, 10.1016/j.neuroimage.2004.01.004, 15110012CrossRefPubMed
40.
go back to reference Coppola G, Ambrosini A, Di Clemente L, Magis D, Fumal A et al (2007) Interictal abnormalities of gamma band activity in visual evoked responses in migraine: an indication of thalamocortical dysrhythmia? Cephalalgia 27:1360–1367, 1:STN:280:DC%2BD2snpsFalsg%3D%3D, 10.1111/j.1468-2982.2007.01466.x, 17986271CrossRefPubMed Coppola G, Ambrosini A, Di Clemente L, Magis D, Fumal A et al (2007) Interictal abnormalities of gamma band activity in visual evoked responses in migraine: an indication of thalamocortical dysrhythmia? Cephalalgia 27:1360–1367, 1:STN:280:DC%2BD2snpsFalsg%3D%3D, 10.1111/j.1468-2982.2007.01466.x, 17986271CrossRefPubMed
41.
go back to reference Panconesi A (2008) Serotonin and migraine: a reconsideration of the central theory. J Headache Pain 9:267–276, 1:CAS:528:DC%2BD1cXhtVyqurnI, 10.1007/s10194-008-0058-2, 18668197PubMedCentralCrossRefPubMed Panconesi A (2008) Serotonin and migraine: a reconsideration of the central theory. J Headache Pain 9:267–276, 1:CAS:528:DC%2BD1cXhtVyqurnI, 10.1007/s10194-008-0058-2, 18668197PubMedCentralCrossRefPubMed
42.
go back to reference Llinás RR, Ribary U, Jeanmonod D, Kronberg E, Mitra PP (1999) Thalamocortical dysrhythmia: A neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc Natl Acad Sci USA 96:15222–15227, 10.1073/pnas.96.26.15222, 10611366PubMedCentralCrossRefPubMed Llinás RR, Ribary U, Jeanmonod D, Kronberg E, Mitra PP (1999) Thalamocortical dysrhythmia: A neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc Natl Acad Sci USA 96:15222–15227, 10.1073/pnas.96.26.15222, 10611366PubMedCentralCrossRefPubMed
43.
go back to reference Llinás RR, Steriade M (2006) Bursting of thalamic neurons and states of vigilance. J Neurophysiol 95:3297–3308, 10.1152/jn.00166.2006, 16554502CrossRefPubMed Llinás RR, Steriade M (2006) Bursting of thalamic neurons and states of vigilance. J Neurophysiol 95:3297–3308, 10.1152/jn.00166.2006, 16554502CrossRefPubMed
44.
go back to reference Mesulam MM (1990) Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Ann Neurol 28:597–613, 1:STN:280:DyaK3M%2Fotlejuw%3D%3D, 10.1002/ana.410280502, 2260847CrossRefPubMed Mesulam MM (1990) Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Ann Neurol 28:597–613, 1:STN:280:DyaK3M%2Fotlejuw%3D%3D, 10.1002/ana.410280502, 2260847CrossRefPubMed
45.
go back to reference Levine M, Carlton S, Becker D, Miller J, Hayes R (1982) Encoding of arterial CO2 tensions by neurons in the region of the locus ceruleus in the cat. In: Heistad DD, Marcus ML (eds) Cerebral blood flow. North-Holland, Amsterdam, pp 503–508 Levine M, Carlton S, Becker D, Miller J, Hayes R (1982) Encoding of arterial CO2 tensions by neurons in the region of the locus ceruleus in the cat. In: Heistad DD, Marcus ML (eds) Cerebral blood flow. North-Holland, Amsterdam, pp 503–508
46.
go back to reference Haxhiu MA, Tolentino-Silva F, Pete G, Kc P, Mack SO (2001) Monoaminergic neurons, chemosensation and arousal. Respir Physiol 129:191–209, 1:CAS:528:DC%2BD38XptVyhug%3D%3D, 10.1016/S0034-5687(01)00290-0, 11738654CrossRefPubMed Haxhiu MA, Tolentino-Silva F, Pete G, Kc P, Mack SO (2001) Monoaminergic neurons, chemosensation and arousal. Respir Physiol 129:191–209, 1:CAS:528:DC%2BD38XptVyhug%3D%3D, 10.1016/S0034-5687(01)00290-0, 11738654CrossRefPubMed
47.
go back to reference Reddy SV, Yaksh TL, Anderson RE, Sundt TM (1986) Effect in cat of locus coeruleus lesions on the response of cerebral blood flow and cardiac output to altered paCO2. Brain Res 365:278–288, 1:STN:280:DyaL287jt1OhsA%3D%3D, 10.1016/0006-8993(86)91639-2, 3004658CrossRefPubMed Reddy SV, Yaksh TL, Anderson RE, Sundt TM (1986) Effect in cat of locus coeruleus lesions on the response of cerebral blood flow and cardiac output to altered paCO2. Brain Res 365:278–288, 1:STN:280:DyaL287jt1OhsA%3D%3D, 10.1016/0006-8993(86)91639-2, 3004658CrossRefPubMed
48.
go back to reference Petroff OA, Prichard JW, Behar KL, Rothman DL, Alger JR et al (1985) Cerebral metabolism in hyper- and hypocarbia: 31P and 1H nuclear magnetic resonance studies. Neurology 35:1681–1688, 1:CAS:528:DyaL28XkvVWmtg%3D%3D, 2933595CrossRefPubMed Petroff OA, Prichard JW, Behar KL, Rothman DL, Alger JR et al (1985) Cerebral metabolism in hyper- and hypocarbia: 31P and 1H nuclear magnetic resonance studies. Neurology 35:1681–1688, 1:CAS:528:DyaL28XkvVWmtg%3D%3D, 2933595CrossRefPubMed
49.
go back to reference Judit A, Sándor PS, Schoenen J (2000) Habituation of visual and intensity dependence of auditory evoked cortical potentials tends to normalize just before and during the migraine attack. Cephalalgia 20:714–719, 1:STN:280:DC%2BD3M7nvFantQ%3D%3D, 11167900CrossRefPubMed Judit A, Sándor PS, Schoenen J (2000) Habituation of visual and intensity dependence of auditory evoked cortical potentials tends to normalize just before and during the migraine attack. Cephalalgia 20:714–719, 1:STN:280:DC%2BD3M7nvFantQ%3D%3D, 11167900CrossRefPubMed
Metadata
Title
Changes in visual-evoked potential habituation induced by hyperventilation in migraine
Authors
Gianluca Coppola
Antonio Currà
Simona Liliana Sava
Alessia Alibardi
Vincenzo Parisi
Francesco Pierelli
Jean Schoenen
Publication date
01-12-2010
Publisher
Springer Milan
Published in
The Journal of Headache and Pain / Issue 6/2010
Print ISSN: 1129-2369
Electronic ISSN: 1129-2377
DOI
https://doi.org/10.1007/s10194-010-0239-7

Other articles of this Issue 6/2010

The Journal of Headache and Pain 6/2010 Go to the issue