Intensity Dependence of Auditory Evoked Potentials Is Pronounced in Migraine: An Indication of Cortical Potentiation and Low Serotonergic Neurotransmission?
[en] Migraine is associated with stimulus hypersensitivity, increased evoked cortical responses, and abnormal 5-HT levels in peripheral blood. We studied cortical auditory evoked potentials (AEPs) between attacks in 35 patients suffering from migraine without aura (MO, n = 25) or with aura (MA, n = 10) and in 25 healthy volunteers. Binaural tones were delivered at 40, 50, 60, and 70 dB sensation level (SL) in a pseudorandomized order. The intensity dependence of the auditory N1-P2 component was significantly greater in MO (p = 0.003) and MA (p = 0.02) patients than in healthy controls, resulting in a much steeper amplitude/stimulus intensity function slope. When three sequential blocks of 40 averaged responses were analyzed at the 40- and 70-dB SL intensities, N1-P2 amplitude decreased in second and third blocks at both intensities in controls, but increased in migraineurs, a difference that was significant in both blocks for the 70-dB SL stimulus. The strong interictal dependence of AEPs on stimulus intensity may thus be due to potentiation (instead of habituation) of the response during repetition of the high-intensity stimulation. In concordance with previous studies of visual evoked potentials, these results confirm that migraine is characterized between attacks by an abnormality of cortical information processing, which might be a consequence of low 5-HT transmission and favor cortical energy demands.
Disciplines :
Neurology Neurosciences & behavior
Author, co-author :
Wang, W.
Timsit-Berthier, M.
Schoenen, Jean ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Neuro-anatomie
Language :
English
Title :
Intensity Dependence of Auditory Evoked Potentials Is Pronounced in Migraine: An Indication of Cortical Potentiation and Low Serotonergic Neurotransmission?
Publication date :
May 1996
Journal title :
Neurology
ISSN :
0028-3878
eISSN :
1526-632X
Publisher :
Lippincott Williams & Wilkins, United States - Maryland
Moskowitz MA. The visceral organ brain: implications for the pathophysiology of vascular head pain. Neurology 1991;41: 182-186.
Goadsby PJ, Edvinsson L, Ekman R. Vasoactive peptide release in the extracerebral circulation of humans during migraine headache. Ann Neurol 1990;28:183-187.
Hardebo JE. A cortical excitatory wave may cause both the aura and the headache of migraine. Cephalalgia 1992;12:75-80.
Lauritzen M. Pathophysiology of the migraine aura: the spreading depression theory. Brain 1994;117:199-210.
Lehtonen JB. Visual evoked potentials for single flashes and flickering light in migraine. Headache 1974;14:1-12.
Mac Lean C, Appenzeller O, Cordoudo JT, Rhodes J. Flash evoked potential in migraine. Headache 1975; 14:193-198.
Connolly JF, Gawel M, Clifford Rose F. Migraine patients exhibit abnormalities in the visual evoked potential. J Neurol Neurosurg Psychiatry 1982;45:464-467.
Nyrke T, Lang AH. Spectral analysis of visual potentials evoked by sine wave modulated light in migraine. Electroencephalogr Clin Neurophysiol 1982;53:436-442.
Gawel M, Connolly JF, Clifford Rose F. Migraine patients exhibit abnormalities in the visual evoked potential. Headache 1983;23:49-52.
Diener HC, Ndosi NK, Koletzki E, Langohr HD. Visual evoked potentials in migraine. In: Pfaffenrath V, Lundberg PJ, Sjaastad O, eds. Updating in headache. Berlin: Springer Verlag, 1984:439-465.
Schoenen J, Maertens A, Timsit-Berthier M, Timsit M. Contingent negative variation (CNV) as a diagnostic and physiopathologic tool in headache patients. In: Clifford Rose F, ed. Proceedings of the 5th International Migraine Symposium, London, 1984. Basel: Karger, 1985:17-25.
Böcker KBE, Timsit-Berthier M, Schoenen J, Brunia CHM. Contingent negative variation in migraine. Headache 1990;30: 604-609.
Kropp P, Gerber WD. Is increased amplitude of contingent negative variation in migraine due to cortical hyperactivity or to reduced habituation? Cephalalgia 1993;13:37-41.
Schoenen J, Wang W, Albert A, Delwaide PJ. Potentiation instead of habituation characterizes visual evoked potentials in migraine patients between attacks. Eur J Neurol 1995;2: 115-122.
Thompson RF, Berry SD, Rinaldi PC, Berger TW. Habituation and orienting reflex: the dural-process theory revised. In: Kimmel HD, van Olst EH, Orlebeke JF, eds. The orienting reflex in humans. Hillsdale, NJ: Lawrence Erlbaum Associates, 1979:21-60.
Hegerl U, Juckel G. Intensity dependence of auditory evoked potentials as an indicator of central serotonergic neurotransmission: a new hypothesis. Biol Psychiatry 1993;33:173-187.
Buchsbaum MS, Silverman J. Stimulus intensity control and the cortical evoked response. Psychosom Med 1968;30:12-22.
Buchsbaum MS, Pfefferbaum A. Individual differences in stimulus intensity response. Psychophysiology 1971;8:600-611.
von Knorring L, Monakhov K, Perris C. Augmenting/reducing: an adaptive switch mechanism to cope with incoming signals in healthy subjects and psychiatric patients. Neuropsychobiology 1978;4:150-179.
von Knorring L, Perris C. Biochemistry of augmenting/reducing response in visual evoked potentials. Neuropsychobiology 1981;7:1-8.
Buchsbaum MS, Haier RJ, Johnson J. Augmenting and reducing: individual differences in evoked potentials. In: Gale A, Edwards JA, eds. Physiological correlates of human behavior, vol 3. London: Academic Press, 1983:117-138.
Anthony M, Hinterberger H, Lance JW. The possible relationship of serotonin to the migraine syndrome. In: Friedman AP, ed. Research and clinical studies in headache, vol 2. New York: Karger, 1969:29-59.
Sicuteri F, Bussone G, Anselmi B, Del Bianco PL. An enzyme (MAO) defect in platelets in migraine. In: Friedman AP, ed. Research and clinical studies in headache, vol 3. Basel: Karger, 1972:245-251.
Ferrari MD. Biochemistry of migraine. Pathol Biol (Paris) 1992;40:284-292.
International Headache Society. Classification and diagnostic criteria for headache disorders, cranial neuralgias and facial pain. Cephalalgia 1988;8(suppl 7):1-96.
Jasper HH. The ten-twenty electrode system of the International Federation. Electroencephalogr Clin Neurophysiol 1958;10:371-375.
Scherg M, Vajsar J, Picton TW. A source analysis of the late human auditory evoked potentials. J Cogn Neurosci 1989;1: 336-355.
Bruneau N, Barthelemy C, Jouve J, Lelord G. Frontal auditory-evoked potential augmenting-reducing and urinary homovanillic acid. Neuropsychobiology 1986;16:78-84.
Hegerl U, Prochno I, Ulrich G, Müller-Oerrlinghausen B. Are auditory evoked potentials suitable for predicting the response to lithium prophylaxis? A study on the effects of repeated measurement, age, gender, and personality on the amplitude/stimulus intensity function in healthy volunteers. Pharmacopsychiatry 1988;21:329-330.
Hegerl U, Prochno I, Ulrich G, Müller-Oerlinghausen B. Sensation seeking and auditory evoked potentials. Biol Psychiatry 1989;25:179-190.
Hegerl U, Gallinat J, Mrowinski D. Intensity dependence of auditory evoked dipole source activity. Int J Psychophysiol 1994;17:1-13.
Buchsbaum MS, Goodwin F, Murhy D, Borge G. AER in affective disorders. Am J Psychiatry 1971;128:51-57.
Hegerl U, Ulrich G, Müller-Oerlingerhausen B. Auditory evoked potentials and response to lithium prophylaxis. Pharmacopsychiatry 1987;20:213-216.
Hegerl U, Herrmann WM. Event-related potentials and the prediction of differential drug response in psychiatry. Neuropsychobiology 1990;23:99-108.
Merikangas KR, Angst J, Isler H. Migraine and psychopathology: results of the Zurich cohort study of young adults. Arch Gen Psychiatry 1990;47:849-853.
Breslau N, Davies GC. Migraine, psychiatric disorders and suicide attempts: an epidemiological study of young adults. Psychiatry Res 1991;37:11-23.
Coursey RD, Buchsbaum MS, Frankel BL. Personality measures and evoked response in chronic insomniacs. J Abnorm Psychol 1975;84:239-249.
Roth WT, Pfefferbaum A, Kelly AF, Berger PA, Kopell BS. Auditory event-related potentials in schizophrenia and depression. Psychiatry Res 1981;4:199-212.
Juckel G, Schmidt LG, Rommelspacher H, Hegerl U. The tridimensional personality questionnaire and the intensity dependence of auditory evoked dipole source activity. Biol Psychiatry 1995;37:311-317.
Passchier J, Andrasik F. Migraine: psychological factors. In: Olesen J, Tfelt-Hansen P, Welch KMA, eds. The headaches. New York: Raven Press, 1993:233-240.
Ginsburg N, Pollack-Fels S. Headache and sensation seeking. Psychol Rep 1991;68:615-619.
Lutzenberger W, Schandry R, Birbaumer N. Habituation of the components of the AEP to stimuli of different intensities. In: Kimmel HD, van Olst EH, Orlebeke JF, eds. The orienting reflex in humans. Hillsdale, NJ: Lawrence Erlbaum Associates, 1979:123-128.
Kennard C, Gawel M, Rudolf N, Clifford Rose F. Visual evoked potentials in migraine subjects. In Friedman AP, Granger ME, eds. Research and clinical studies in headache. Basel: Karger, 1978;6:73-80.
Ellertsen B, Hammerborg D. Psychophysiological response pattern in migraine patients. Cephalalgia 1982;2:19-24.
Sappey-Marinier D, Galabrese G, Fein G, Hugg JW, Biggins C, Weiner MW. Effect of photic stimulation on human visual cortex lactate and phosphates using 1H and 31P magnetic resonance spectroscopy. J Cereb Blood Flow Metab 1992;12: 584-592.
Kandel ER. Cellular mechanisms of learning and biological basis of individuality. In: Kandel EC, Schwartz JH, Jessell TM, eds. Principles of neural science. New York: Elsevier, 1992:1009-1031.
Sokolov EN. Perception and the conditioned reflex. Oxford: Pergamon, 1963.
Thompson RF, Spencer WA. Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol Rev 1966;7:16-43.
Lukas JH, Siegel J. Cortical mechanisms that augment or reduce evoked potentials in cats. Science 1977;198:73-75.
Gottfries C, von Knorring L, Perries C. Neurophysiological measures related to levels of 5-HIAA, HVA, and tryptophan in CSF of psychiatric patients. Neuropsychobiology 1976;2:1-8.
Mesulam M-M. Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Ann Neurol 1990;28:597-613.
Jacobs BL, Azmitia EC. Structure and function of the brain serotonin system. Physiol Rev 1992;72:165-229.
Schoenen J. Pathogenesis of migraine: the biobehavioral and hypoxia theories reconciled. Acta Neurol Belg 1994;94:79-86.
Barbiroli B, Montagna P, Cortelli P, et al. Abnormal brain and muscle energy metabolism shown by 31P magnetic resonance spectroscopy in patients affected by migraine with aura. Neurology 1992;42:1209-1214.
Montagna P, Cortelli P, Monari L, et al. 31P-Magnetic resonance spectroscopy in migraine without aura. Neurology 1994; 44:666-668.