Brain, Vol. 122, No. 6, 1147-1155,
June 1999
© 1999 Oxford University Press
Visual evoked potentials in migraine patients: alterations depend on pattern spatial frequency
1 Department of Experimental and Clinical Pharmacology and Toxicology and 2 Department of Neurology, University of Erlangen-Nürnberg, Germany
Correspondence to:
Rieke Oelkers, MD, Department of Child and Adolescent Psychiatry, University of Heidelberg, Blumenstrasse 8, D-69115 Heidelberg, Germany E-mail: rieke_oelkers{at}med.uni-heidelberg.de
| Abstract |
|---|
|
|
|---|
Visual information is conducted by two parallel pathways (luminance- and contour-processing pathways) which are thought to be differentially affected in migraine and can be investigated by means of pattern-reversal visual evoked potentials (VEPs). Components and habituation of VEPs at four spatial frequencies were compared between 26 migraineurs (13 without aura, MO; 13 with aura, MA) and 28 healthy volunteers. Migraineurs were recorded in the headache-free interval (at least 72 h before and after an attack). Five blocks of 50 responses to chequerboards of 0.5, 1, 2 and 4 cycles per degree (c.p.d.) were sequentially averaged and analysed for latency and amplitude. Differences in VEPs were dependent on spatial frequency. Only when small checks were presented, i.e. at high spatial frequency (2 and 4 c.p.d.), was the latency of N2 significantly prolonged in MA and did it tend to be delayed in MO subjects. Habituation behaviour was not significantly different between groups under the stimulating conditions employed. Prolonged N2 latency might be explained by the lack or attenuation of a contour-specific component N130 in migraineurs, indicating an imbalance of the two visual pathways with relative predominance of the luminance-processing Y system. These results reflect an interictally persisting dysfunction of precortical visual processing which might be relevant in the pathophysiology of migraine.
migraine; visual evoked potential; pattern spatial frequency; habituation; pathophysiology
c.p.d. = cycles per degree; d.f. = degrees of freedom; MA = migraine with aura; MO = migraine without aura; VAS = visual analogue scale; VEP = visual evoked potential
| Introduction |
|---|
|
|
|---|
Visual symptoms and photophobia are common features of migraine, but are not exclusively confined to attacks. Hypersensitivity to environmental light (Hay et al., 1994
One important aspect of information-processing dysfunction is reduced habituation to stimuli, which has been found, for example, for visual evoked potentials (VEP) and contingent negative variation (Schoenen et al., 1986
, 1995
; Afra et al., 1998
). Deficient habituation in migraineurs, i.e. the absence of a decrement in amplitude over time, might partly account for the increased amplitudes reported in previous VEP studies (Gawel et al., 1983
; Diener et al., 1989
; Shibata et al., 1997
). Although several studies have investigated VEPs in migraineurs, results remain controversial (Kennard et al., 1978
; Winter and Cooper, 1985; Polich et al., 1986
; Mariani et al., 1988
; Drake et al., 1990
; Ristanovic et al., 1990
; Moreira and Dantas, 1994). This might be due to methodological differences with regard to stimulated field, contrast, spatial and temporal frequency of the patterns used. Check size, i.e. spatial frequency, influences the components and habituation behaviour of pattern-reversal VEPs (Harter and White, 1968
, 1970
; Peachey et al., 1994
). This is linked to the different involvement of two parallel pathways, the luminance-processing Y system and the contour-processing X system. Affection of these two pathways in migraine has been proposed (Diener et al., 1989
). Clinical evidence for this hypothesis has come from psychophysical tests in which migraineurs showed reduced performance in precortical spatial and temporal visual processing (Coleston et al., 1993, 1994
). Pathway affection has yet not been investigated using electrophysiological methods, since all previous VEP studies have been performed using only a single check size for stimulation. The aim of the present study was therefore to clarify the affection and interaction of the X and Y systems in migraine by means of pattern-reversal VEP. For this purpose, VEP components and habituation behaviour at four spatial frequencies were compared between migraineurs and healthy controls.
| Methods |
|---|
|
|
|---|
Subjects
Fifty-four subjects (43 females, 11 males) participated in the study: 28 healthy volunteers (controls; 18 females, 10 males; mean age ± SD, 27.1 ± 4.1 years) and 26 migraineurs (25 females, 1 male; mean age ± SD, 29.1 ± 5.9 years). Thirteen had migraine without aura (MO, code 1.1) and 13 had migraine with aura (MA, code 1.2) (Headache Classification Committee of the International Headache Society, 1988
Experimental design and recordings
Black-and-white chequerboard patterns (contrast >99%, reversal frequency 1 Hz) were binocularly presented on a video screen subtending 12x15° of visual angle. Subjects were instructed to fixate on a red point 1.5 cm below and in the middle of the upper border of the screen, as described by Diener and colleagues (Diener et al., 1989
). Spatial frequencies (0.5, 1, 2 and 4 c.p.d.) were applied in increasing order, i.e. proceeding from large to small checks. Each spatial frequency was presented in five consecutive blocks of 50 responses each. Presentation of different spatial frequencies was separated by at least 3 min (time for psychophysical rating) to allow recovery from visual stimulation. During the experiment the subjects were comfortably seated, and white noise via headphones (50 dB SPL) was used for acoustic shielding. EEG was recorded from one position of the international 10/20 system (Oz), referenced to linked earlobes (A1 + A2) using surface AgAgCl electrodes. After analogue-to-digital conversion, stimulus-linked EEG segments (sampling time 350 ms, prestimulus baseline 100 ms, sampling frequency 250 Hz, band-pass 0.0130 Hz) were evaluated off-line and automated artefact rejection (single responses contaminated by eye-blinks or muscle artefacts >40 µV) was applied before averaging. Possible eye-blink artefacts were registered from Fp2/(A1 + A2). The five consecutive blocks of each spatial frequency were analysed for peak latencies (P0, N1, P1, N2) and peak-to-peak amplitudes of the maximal negative or positive deflections (N1P1, P1N2) were determined by visual inspection of each averaged recording. In addition, subjects had to rate (visual analogue scale, VAS) (i) the visual discomfort provoked by each pattern; (ii) the acoustic discomfort provoked by the white noise used for acoustic shielding; (iii) aversive effects (eye-ache, queasy feeling, headache, nausea, dizziness); and (iv) the number of illusions (colours, shadows, grids, etc.) after each block.
Data analysis
Statistical analysis was carried out using SPSS for windows, version 7.4. Results were compared by multiway analysis of variance (MANOVA) for repeated measures; the within-subject factor was block [degrees of freedom (d.f.) = 4) and the between-subject factor was group (see below)]. Prior to this, the between-subject factor gender (d.f. = 1) was tested in a separate analysis of variance; no significant influence on VEP parameters and subjective ratings could be detected. After that, the between-subject factor of group was first set to migraine (migraineurs = MA and MO versus controls, d.f. = 1) and then to aura (MA versus MO versus controls, d.f. = 2) to detect differences between the two groups of migraineurs. When appropriate, the number of degrees of freedom was adjusted according to Greenhouse and Geisser. The corresponding
values and the corrected significance levels are reported. Post hoc analysis was carried out by Scheffé's test. Habituation was calculated using a relative value, and amplitudes of blocks 25 were divided by the amplitude of block 1. Subjective ratings (discomfort VAS, colour illusion VAS, figure illusion VAS and number of aversive effects) were compared using non-parametric tests (KruskalWallis test, MannWhitney U test). The
level was set to 0.05. If not indicated otherwise, group data are presented as mean ± standard error of the mean.
| Results |
|---|
|
|
|---|
VEP
Latency
Grand means of the VEP recordings of the first block at four different spatial frequencies of MA, MO and controls are presented in Fig. 1
|
Migraineurs exhibited longer latencies of the N2 component than healthy controls when small checks were presented, i.e. at high spatial frequency (Table 1
|
|
Latencies of the early VEP components (P0, N1, P1) also tended to be prolonged in MA patients, but only a few differences between MA, MO and control subjects (between-subject factor aura) reached weak significance. P0 tended to be prolonged in MA patients; differences were significant at 0.5 and 2 c.p.d. [0.5 c.p.d., first block (ms), MA 52.3 ± 4.7, MO 49.5 ± 2.5, controls 50.6 ± 2.5; F(2,51) = 3.3, P = 0.046; 2 c.p.d.: first block (ms), MA 65.9 ± 3.7, MO 56.0 ± 3.5, controls 57.3 ± 2.6; F(2,51) = 6.3, P = 0.003]. At 2 c.p.d., weakly significant aura x block interaction occurred [F(4,948) = 2.301,
= 0.618, P = 0.049], indicating more pronounced latency prolongation in MA over the five blocks. N1 latency was significantly different between groups at 1 c.p.d. [first block (ms): MA 89.2 ± 1.5, MO 80.6 ± 2.9, controls 84.1 ± 1.5; F(2,51) = 3.5, P = 0.037] and P1 latency at 2 c.p.d. [first block (ms): MA 124.6 ± 1.2, MO 120.0 ± 2.1, controls 120.4 ± 1.4; F(2,51) = 3.4, P = 0.041]. For the factor migraine, latencies of the early VEP components (P0, N1, P1) were not significantly different.
Amplitude
The peak-to-peak amplitudes (N1P1, P1N2) were consistently higher in migraineurs at all spatial frequencies tested, N1P1 ranging from 23.3 to 29.9 µV in MO patients and from 19.2 to 30.9 µV in MA patients compared with a range from 17.8 to 26.0 µV in controls. Amplitude augmentation in migraineurs was marked at low spatial frequencies. P1N2 differences reached statistical significance at 0.5 c.p.d. for the between-subject factor migraine [first block (µV): MA 22.2 ± 3.4, MO 22.4 ± 3.6, controls 17.4 ± 1.4; F(1,51) = 4.6, P = 0.038] and at 1 c.p.d. for aura [first block (µV): MA 33.0 ± 3.8, MO 27.6 ± 3.3, controls 25.7 ± 1.7; F(2,51) = 3.6, P = 0.036].
Habituation
Habituation was calculated using a relative value [amplitude (block 25)/amplitude (block 1)]. In migraineurs and controls amplitude decreased over blocks when the smallest check size was presented, indicating habituation at high spatial frequency (4 c.p.d.). When large checks were presented (0.5 c.p.d.), amplitude tended to increase over blocks in MA patients whereas MO patients and controls showed stable or slightly declining responses. However, group differences did not reach statistical significance at any spatial frequency either for the between-subject factor migraine (d.f. = 1) or for aura (d.f. = 2) (Fig. 3
).
|
Psychophysical rating
Illusions
Migraineurs reported more colour and figure illusions at all spatial frequencies (Fig. 4
|
Aversive effects
The percentage of subjects reporting one to three aversive effects was augmented at high spatial frequencies in migraineurs but not in control subjects. Differences were statistically significant at 2 and 4 c.p.d. (MannWhitney U test, grouping factor migraine: df. = 1, P = 0.002 and P = 0.001, respectively; KruskalWallis test, grouping factor aura: d.f. = 2, P = 0.005 at 2 and 4 c.p.d.).
Discomfort of visual and acoustic stimulation
MA patients tended to experience more visual discomfort at 2 and 4 c.p.d. (data not shown), but group differences were not statistically significant either for the factor migraine (MannWhitney U test, d.f. = 1) or for aura (KruskalWallis test, d.f. = 2). Rating of the white noise used for acoustic shielding, however, revealed significantly higher discomfort in migraineurs at high spatial frequencies (MannWhitney U test, grouping factor migraine: d.f. = 1, P = 0.011 at 2 c.p.d., P = 0.012 at 4 c.p.d.; KruskalWallis test, grouping factor aura: d.f. = 2, P = 0.036 at 2 c.p.d., P = 0.015 at 4 c.p.d.).
| Discussion |
|---|
|
|
|---|
Up to now, no study has systematically investigated VEPs at different spatial frequencies in migraine. Most studies have focused on latencies of the stable early components and patterns of low spatial frequencies, i.e.
1 c.p.d. (Kennard et al., 1978
VEP parameters vary as a function of check size. Two visual pathways are involved to different degrees: the X system and the Y system (Harter and White, 1968
, 1970
). Large patterns (i.e. low spatial frequency, 0.5 and 1 c.p.d.) are mainly conducted by the Y system, which processes movement and luminance. In contrast, the X system processes contrast and contour. For small patterns both the X system and the Y system are involved (Kulikowski, 1977
, 1978
). These two pathways have properties equivalent to two spatiotemporal filters (ST1 and ST2) on visual stimuli. ST1 is linked to the X-type mechanism and is stimulated by spatially modulated background gratings with a peak response at 48 c.p.d. and low temporal frequency (non-flickering). ST2 has low-pass properties for spatial frequencies (peak 1 c.p.d.) and band-pass properties for temporal frequencies (peak 1020 Hz) like the Y-type mechanism (Holliday and Ruddock, 1983
). The Y system receives input mainly from the retinal periphery via the magnocellular pathway (dorsal layers of lateral geniculate nucleus, lateral geniculate nucleus) and is very sensitive to contrast (Kubová et al., 1995
). The X system receives input mainly from foveal and perifoveal areas via the parvocellular pathway (ventral layers of the lateral geniculate nucleus) and requires higher luminous intensities.
The P1 component of pattern-reversal VEPs is attributed to the X system. In contrast, the N2 component is ascribed mainly to the Y system (Kubová et al., 1995
). Latencies of all VEP components increase with increasing spatial frequency, but prolongation of N2 is partly compensated for by the appearance of an earlier contour-specific negative component called N130 (Wenzel, 1984
). This component interferes with the Y-dependent N180, and the resulting N2 is a superposition of N130 and N180. N130 is characteristic of potentials evoked by small checks and might be ascribed to the X system (Wenzel, 1984
). In healthy subjects, N130 predominates when small checks are presented and is therefore important for `normal' N2 latencies at high spatial frequency. Delayed N2 latency for these check sizes in migraineurs may be due to an attenuated or absent N130 and/or a relatively predominant N180 (Fig. 5
). This might reflect an imbalance of the two visual pathways with relative predominance of the luminance-dependent Y system. Intrinsic abnormalities in the connectivity of the magnocellular (Y) and parvocellular (X) precortical visual pathways (Coleston et al., 1994
), possibly due to impairment of GABAergic inhibitory interneurons (Chronicle and Mulleners, 1994
) and/or altered dopaminergic transmission, may be responsible.
|
This concept of XY imbalance also makes it clear why marked latency group differences are limited to the presentation of small patterns that stimulate both pathways. Our results are in line with those of others that suggest normal N2 latencies for migraineurs under Y-stimulating conditions, i.e. when large checks are applied (Winter and Cooper, 1985; Polich et al., 1986
The barely changed latencies of the early VEP components P0, N1 and P1 in migraineurs may be explained by the generally greater stability of the early VEP components affected primarily by morphological changes in the optic nerve and the central pathways (Ellingson et al., 1973
). Our results are basically in accordance with those of other authors (Winter and Cooper, 1985; Polich et al., 1986
; Mariani et al., 1988
; Drake et al., 1990
; Ristanovic et al., 1990
; Schoenen et al., 1995
; Tagliati et al., 1995
).
Different involvement of the X and the Y systems is also proposed to play a role in habituation behaviour with respect to pattern-reversal stimulation. In normal subjects, clear habituation is found only when small checks are presented. In contrast, nearly stable responses are characteristic of low spatial frequencies, i.e. Y-stimulating conditions (Peachey et al., 1994
). This is consistent with our findings. No statistically significant differences were found between MA, MO and control subjects. This is in contrast to previous studies describing deficient habituation in migraineurs at high spatial frequency (Schoenen et al., 1995
; Afra et al., 1998
). The discrepancy might be explained by the different stimulating conditions, with a greater proportion of Y stimulation compared with our design due to higher temporal frequency and lower pattern contrast. Low pattern contrast is known to increase habituation effects (Thompson and Spencer, 1966
). As normal subjects fail to habituate under Y-stimulating conditions, the previously described deficient habituation to pattern stimuli in migraineurs (Schoenen et al., 1995
; Afra et al., 1998
) might be linked to the proposed predominance of the Y system. This would also be consistent with the statistically non-significant tendency to increasing amplitude that we found in MA patients at 0.5 c.p.d.
Habituation behaviour in migraine seems to be affected in a complex way, depending on stimulating conditions, rather than being generally impaired. A predominant Y system might contribute to altered habituation behaviour under specific stimulating conditions. Further research in which these conditions are varied (contrast, spatial and temporal frequency, time course of repeated series of habituation) is necessary for clarification.
Spatial frequency also influenced the psychophysical ratings in our study, so subjective discomfort and aversive effects similar to symptoms of migraine attacks (eye-ache, queasy feeling, headache, nausea, dizziness) are particularly reported at high spatial frequencies in the migraineur group. At present, it is not evident how these subjective perceptions are related to the prolongation of N2 latency. However, the parallelism of objective and subjective findings might indicate that XY imbalance plays a role in migraine pathophysiology and is probably involved in triggering migraine attacks.
In summary, for the first time a prolongation of N2 latency in migraineurs was shown at high spatial frequencies, i.e. when small checks were presented. Habituation behaviour was not different between groups. The prolongation of N2 latency argues in favour of an imbalance of the luminance-processing Y system and the contour-processing X system. Interictal Y predominance might increase sensitivity to visual stimuli and thereby be relevant in migraine pathophysiology.
| Acknowledgments |
|---|
We thank Hanns Ulrich Zeilhofer for helpful discussion and the graphics in Fig. 1
| References |
|---|
|
|
|---|
Afra J, Cecchini AP, De Pasqua V, Albert A, Schoenen J. Visual evoked potentials during long periods of pattern-reversal stimulation in migraine. Brain 1998; 121: 23341.
Andrasik F, Kabela E, Quinn S, Attanasio V, Blanchard EB, Rosenblum EL. Psychological functioning of children who have recurrent migraine. Pain 1988; 34: 4352.[Web of Science][Medline]
Bille BS. Migraine in school children. Acta Paediatr (Upps) 1962; 51 Suppl 136: 1151.
Chronicle E, Mulleners W. Might migraine damage the brain? [Review]. Cephalalgia 1994; 14: 4158.[Web of Science][Medline]
Coleston DM, Kennard C. Visual changes in migraine: indications of cortical dysfunction. Cephalalgia 1993; 13 Suppl 13: 11.
Coleston DM, Chronicle E, Ruddock KH, Kennard C. Precortical dysfunction of spatial and temporal visual processing in migraine. J Neurol Neurosurg Psychiatry 1994; 57: 120811.
Diener HC, Scholz E, Dichgans J, Gerber WD, Jäck A, Bille A, et al. Central effects of drugs used in migraine prophylaxis evaluated by visual evoked potentials. Ann Neurol 1989; 25: 12530.[Web of Science][Medline]
Drake ME, Pakalnis A, Hietter SA, Padamadan H. Visual and auditory evoked potentials in migraine. Electromyogr Clin Neurophysiol 1990; 30: 7781.[Medline]
Ellingson RJ, Lathrop GH, Danahy T, Nelson B. Variability of visual evoked potentials in human infants and adults. Electroencephalogr Clin Neurophysiol 1973; 34: 11324.[Web of Science][Medline]
Gawel M, Connolly JF, Rose FC. Migraine patients exhibit abnormalities in the visual evoked potential. Headache 1983; 23: 4952.[Web of Science][Medline]
Gerber WD. Social and behavioral factors in children suffering from headache: the role of need for achievement and family interaction. Cephalalgia 1987; 7 Suppl 7: 3678.
Gerber WD, Schoenen J. Biobehavioral correlates in migraine: the role of hypersensitivity and information-processing dysfunction. [Review]. Cephalalgia 1998; 18 Suppl 21: 511.
Harter MR, White CT. Effects of contour sharpness and check-size on visually evoked cortical potentials. Vision Res 1968; 8: 70111.[Web of Science][Medline]
Harter MR, White CT. Evoked cortical responses to checkerboard patterns: effect of check-size as a function of visual acuity. Electroencephalogr Clin Neurophysiol 1970; 28: 4854.[Web of Science][Medline]
Hay KM, Mortimer MJ, Barker DC, Debney LM, Good PA. 1044 women with migraine: the effect of environmental stimuli. Headache 1994; 34: 1668.[Web of Science][Medline]
Headache Classification Committee of the International Headache Society. Classification and diagnostic criteria for headache disorders, cranial neuralgias and facial pain. Cephalalgia 1988; 8 Suppl 7: 196.
Holliday EI, Ruddock KH. Two spatio-temporal filters in human vision. Biol Cybern 1983; 47: 17390.[Web of Science][Medline]
Kennard C, Gawel M, Rudolph NM, Rose FC. Visual evoked potentials in migraine subjects. Res Clin Stud Headache 1978; 6: 7380.[Medline]
Kropp P, Gerber WD. Contingent negative variationfindings and perspectives in migraine. Cephalalgia 1993; 13: 336.[Web of Science][Medline]
Kubová Z, Kuba M, Spekreijse H, Blakemore C. Contrast dependence of motion-onset and pattern-reversal evoked potentials. Vision Res 1995; 35: 197205.[Web of Science][Medline]
Kulikowski JJ. Separation of occipital potentials related to the detection of pattern and movement. In: Desmedt JE, editor. Visual evoked potentials in man: new developments. Oxford: Clarendon Press; 1977. p. 18496.
Kulikowski JJ. Pattern and movement detection in man and rabbit: separation and comparison of occipital potentials. Vision Res 1978; 18: 1839.[Web of Science][Medline]
Lucas RN. Migraine in twins. J Psychosom Res 1977; 21: 14756.[Web of Science][Medline]
Marcus DA, Soso MJ. Migraine and stripe-induced visual discomfort. Arch Neurol 1989; 46: 112932.
Mariani E, Moschini V, Pastorino G, Rizzi F, Severgnini A, Tiengo M. Pattern-reversal visual evoked potentials and EEG correlations in common migraine patients. Headache 1988; 28: 26971.[Web of Science][Medline]
Moreira Filho PF, Dantas AM. Pattern reversal visual evoked potentials in migraine subjects without aura [see comments]. Arq Neuropsiquiatr 1994; 52: 4848. Comment in: Arq Neuropsiquiatr 1995; 53: 3513.[Medline]
Peachey NS, DeMarco PJ Jr, Ubilluz R, Yee W. Short-term changes in the response characteristics of the human visual evoked potential. Vision Res 1994; 34: 282331.[Web of Science][Medline]
Polich J, Ehlers CL, Dalessio DJ. Pattern-shift visual evoked responses and EEG in migraine. Headache 1986; 26: 4516.[Web of Science][Medline]
Ristanovic D, Martinovic Z, Jovic N. Pattern-reversal visual evoked potentials in children with migraine: a correlation analysis. Neurologija 1990; 39: 18598.[Medline]
Schoenen J, Maertens de Noordhout A, Timsit-Berthier M, Timsit M. Contingent negative variation and efficacy of beta-blocking agents in migraine. Cephalalgia 1986; 6: 22933.[Web of Science][Medline]
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: 11522.[Web of Science]
Shibata K, Osawa M, Iwata M. Pattern reversal visual evoked potentials in classic and common migraine. J Neurol Sci 1997; 145: 17781.[Web of Science][Medline]
Tagliati M, Sabbadini M, Bernardi G, Silvestrini M. Multichannel visual evoked potentials in migraine. Electroencephalogr Clin Neurophysiol 1995; 96: 15.[Medline]
Thompson RF, Spencer WA. Habituation: a model phenomenon for the study of neuronal substrates of behavior. [Review]. Psychol Rev 1966; 73: 1643.[Web of Science][Medline]
van der Kamp W, Maassen VanDenBrink A, Ferrari MD, van Dijk JG. Interictal cortical hyperexcitability in migraine patients demonstrated with transcranial magnetic stimulation. J Neurol Sci 1996; 139: 10610.[Web of Science][Medline]
van der Kamp W, Maassen VanDenBrink A, Ferrari MD, van Dijk JG. Interictal cortical excitability to magnetic stimulation in familial hemiplegic migraine. Neurology 1997; 48: 14624.
Wenzel D. Visuell evozierte Potentiale durch Musterreizung beim Kind. Klinische Anwendung bei Läsionen der afferenten Sehbahn. Stuttgart: Ferdinand Enke; 1984.
Wilkins A, Nimmo-Smith I, Tait A, McManus C, Della Sala S, Tilley A, et al. A neurological basis for visual discomfort. Brain 1984; 107: 9891017.
Wilkins JA, Della Sala S, Somazzi L, Nimmo-Smith I. Age-related norms for the Cambridge Low Contrast Gratings, including details concerning their design and use. Clin Vision Sci 1988; 2: 20112.
Winter AL, Cooper R. Neurophysiological measures of the visual system in classic migraine. In: Clifford Rose F, editor. Migraine. Proceedings of the 5th International Migraine Symposium, London 1984. Basel: Karger; 1985. p. 116.
Wray SH, Mijovic-Prelec D, Kosslyn SM. Visual processing in migraineurs. Brain 1995; 118: 2535.
Received November 25, 1998. Accepted January 18, 1999.
![]()
CiteULike
Connotea
Del.icio.us What's this?
This article has been cited by other articles:
![]() |
W-T Chen, S-J Wang, J-L Fuh, C-P Lin, Y-C Ko, and Y-Y Lin Peri-ictal Normalization of Visual Cortex Excitability in Migraine: an MEG Study Cephalalgia, November 1, 2009; 29(11): 1202 - 1211. [Abstract] [Full Text] [PDF] |
||||
![]() |
D Magis, A Ambrosini, L Bendtsen, M Ertas, H Kaube, J Schoenen, and (EUROHEAD project) Evaluation and Proposal for Optimalization of Neurophysiological Tests in Migraine: Part 1--Electrophysiological Tests Cephalalgia, December 1, 2007; 27(12): 1323 - 1338. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. S. Tibber and A. J. Shepherd Transient Tritanopia in Migraine: Evidence for a Large-Field Retinal Abnormality in Blue-Yellow Opponent Pathways Invest. Ophthalmol. Vis. Sci., November 1, 2006; 47(11): 5125 - 5131. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Shepherd Colour Vision in Migraine: Selective Deficits for S-Cone Discriminations Cephalalgia, June 1, 2005; 25(6): 412 - 423. [Abstract] [Full Text] [PDF] |
||||
![]() |
R Oelkers-Ax, P Parzer, F Resch, and M Weisbrod Maturation of Early Visual Processing Investigated by a Pattern-Reversal Habituation Paradigm is Altered in Migraine Cephalalgia, April 1, 2005; 25(4): 280 - 289. [Abstract] [Full Text] [PDF] |
||||
![]() |
A Ambrosini, A. de Noordhout, P. Sandor, and J Schoenen Electrophysiological Studies in Migraine: A Comprehensive Review of Their Interest and Limitations Cephalalgia, May 1, 2003; 23(1_suppl): 13 - 31. [Abstract] [Full Text] [PDF] |
||||
![]() |
V. Bohotin, A. Fumal, M Vandenheede, P. Gerard, C. Bohotin, A. Maertens de Noordhout, and J. Schoenen Effects of repetitive transcranial magnetic stimulation on visual evoked potentials in migraine Brain, April 1, 2002; 125(4): 912 - 922. [Abstract] [Full Text] [PDF] |
||||
![]() |
K Benedek, J Tajti, M Janaky, L Vecsei, and G Benedek Spatial Contrast Sensitivity of Migraine Patients Without Aura Cephalalgia, March 1, 2002; 22(2): 142 - 145. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. J. Shepherd Increased visual after-effects following pattern adaptation in migraine: a lack of intracortical excitation? Brain, November 1, 2001; 124(11): 2310 - 2318. [Abstract] [Full Text] [PDF] |
||||
![]() |
N Galeotti, C Ghelardini, M Zoppi, E Del Bene, L Raimondi, E Beneforti, and A Bartolini Hypofunctionality of Gi Proteins as Aetiopathogenic Mechanism for Migraine and Cluster Headache Cephalalgia, February 1, 2001; 21(1): 38 - 45. [Abstract] [Full Text] [PDF] |
||||
![]() |
T Sand and J V. Vingen Visual, Long-Latency Auditory and Brainstem Auditory Evoked Potentials in Migraine: Relation to Pattern Size, Stimulus Intensity, Sound and Light Discomfort Thresholds and Pre-Attack State Cephalalgia, November 1, 2000; 20(9): 804 - 820. [Abstract] [Full Text] [PDF] |
||||
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||




grouping factor aura: KruskalWallis test, P < 0.05;
grouping factor aura: KruskalWallis test, P < 0.01.


