Visual input drives increased occipital responsiveness and harmonized oscillations in multiple cortical areas in migraineurs

Mehnert, Jan; Bader, Daniel; Nolte, Guido; May, Arne

doi:10.1016/j.nicl.2019.101815

Cited by 23 publications

(26 citation statements)

References 63 publications

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“…The correlation analysis also showed that both the MEP and the SSEP slope increase with the time elapsed since the last attack increases. Comparable switches depending on the phase of the migraine cycle have been reported for a number of brain studies in migraine: resting MEP threshold [7], visual cortex responsivity [32][33][34], lateral inhibition of the visual [32] and somatosensory [20] cortices, spinal trigeminal nucleus activation [35], brainstem serotonergic receptor binding [36] and thalamic microstructure [37]. All these studies support the concept that the recurrence of migraine attacks is associated with cycling functional and morphological alterations in cortical and subcortical centers.…”

Section: Discussionsupporting

confidence: 70%

Short-latency afferent inhibition and somato-sensory evoked potentials during the migraine cycle: surrogate markers of a cycling cholinergic thalamo-cortical drive?

Lenola

Abagnale

Ferrandes

et al. 2020

Preprint

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Background: Short-latency afferent inhibition (SAI) consists of motor cortex inhibition induced by sensory afferents and depends on the excitatory effect of cholinergic thalamocortical projections on inhibitory GABAergic cortical networks. Given the electrophysiological evidence for thalamo-cortical dysrhythmia in migraine, we studied SAI in migraineurs during and between attacks and searched for correlations with somatosensory habituation, thalamocortical activation, and clinical features.Methods: SAI was obtained by conditioning the transcranial magnetic stimulation-induced motor evoked potential (MEP) with an electric stimulus on the median nerve at the wrist with random stimulus intervals corresponding to the latency of individual somatosensory evoked potentials (SSEP) N20 plus 2, 4, 6, or 8 ms. We recruited 30 migraine without aura patients, 16 between (MO), 14 during an attack (MI), and 16 healthy volunteers (HV). We calculated the slope of the linear regression between the unconditioned MEP amplitude and the 4-conditioned MEPs as a measure of SAI. We also measured SSEP amplitude habituation, and high-frequency oscillations (HFO) as an index of thalamo-cortical activation.Results: Compared to HV, SAI, SSEP habituation and early SSEP HFOs were significantly reduced in MO patients between attacks, but enhanced during an attack. There was a positive correlation between degree of SAI and amplitude of early HFOs in HV, but not in MO or MI. When the two patient groups were pooled, both the MEP SAI slope and the SSEP habituation slope correlated positively with the number of days elapsed since the last migraine attack.Conclusions: The migraine cycle-dependent variations of SAI and SSEP HFOs are further evidence that facilitatory thalamocortical activation (of GABAergic networks in the motor cortex for SAI), likely to be cholinergic, is reduced in migraine at a distance from an attack, but increased ictally.

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Section: Discussionsupporting

confidence: 70%

Short-latency afferent inhibition and somato-sensory evoked potentials during the migraine cycle: surrogate markers of a cycling cholinergic thalamo-cortical drive?

Lenola

Abagnale

Ferrandes

et al. 2020

Preprint

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“…Previous studies have shown that the general time course of migraine attacks normalizes neural functioning during attack and that the abnormalities increase with longer time since attack. [50][51][52][53][54][55][56][57][58] Therefore, not controlling for time since attack may have introduced more noise into the data, reducing the effect of color on visual discomfort in migraine (and the effect might have been even stronger than we have demonstrated). For future studies, careful monitoring of days since or until next migraine attack ought to be recorded.…”

Section: Large and Large Chromaticity Separations For Individuals Wimentioning

confidence: 76%

Cortical Hyper‐Excitability in Migraine in Response to Chromatic Patterns

et al. 2019

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Objective Individuals with migraine exhibit heightened sensitivity to visual input that continues beyond their migraine episodes. However, the contribution of color to visual sensitivity, and how it relates to neural activity, has largely been unexplored in these individuals. Background Previously, it has been shown that, in non‐migraine individuals, patterns with greater chromaticity separation evoked greater cortical activity, regardless of hue, even when colors were isoluminant. Therefore, to investigate whether individuals with migraine experienced increased visual sensitivity, we compared the behavioral and neural responses to chromatic patterns of increasing separation in migraine and non‐migraine individuals. Methods Seventeen individuals with migraine (12 with aura) and 18 headache‐free controls viewed pairs of colored horizontal grating patterns that varied in chromaticity separation. Color pairs were either blue‐green, red‐green, or red‐blue. Participants rated the discomfort of the gratings and electroencephalogram was recorded simultaneously. Results Both groups showed increased discomfort ratings and larger N1/N2 event‐related potentials (ERPs) with greater chromaticity separation, which is consistent with increased cortical excitability. However, individuals with migraine rated gratings as being disproportionately uncomfortable and exhibited greater effects of chromaticity separation in ERP amplitude across occipital and parietal electrodes. Ratings of discomfort and ERPs were smaller in response to the blue‐green color pairs than the red‐green and red‐blue gratings, but this was to an equivalent degree across the 2 groups. Conclusions Together, these findings indicate that greater chromaticity separation increases neural excitation, and that this effect is heightened in migraine, consistent with the theory that hyper‐excitability of the visual system is a key signature of migraine.

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“…Notably, migraine and migraine-induced symptoms have a strong association with anxiety and depression [2]. Additional network circuits have been implicated in migraine pathophysiology and other types of negative emotional and affective processes, including the thalamo-cortical system, based on evidence for altered microstructures and functional connectivities [18]. Nevertheless, few of the currently available studies have specifically revealed abnormal thalamic FC with the visual network and correlations with neuropsychiatric symptoms.…”

Section: Introductionmentioning

confidence: 99%

Impaired intrinsic functional connectivity between the thalamus and visual cortex in migraine without aura

et al. 2019

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Background: Resting-state functional magnetic resonance imaging (fMRI) has confirmed disrupted visual network connectivity in migraine without aura (MwoA). The thalamus plays a pivotal role in a number of pain conditions, including migraine. However, the significance of altered thalamo-visual functional connectivity (FC) in migraine remains unknown. The goal of this study was to explore thalamo-visual FC integrity in patients with MwoA and investigate its clinical significance. Methods: Resting-state fMRI data were acquired from 33 patients with MwoA and 22 well-matched healthy controls. After identifying the visual network by independent component analysis, we compared neural activation in the visual network and thalamo-visual FC and assessed whether these changes were linked to clinical characteristics. We used voxel-based morphometry to determine whether functional differences were dependent on structural differences. Results: The visual network exhibited significant differences in regions (bilateral cunei, right lingual gyrus and left calcarine sulcus) by inter-group comparison. The patients with MwoA showed significantly increased FC between the left thalami and bilateral cunei and between the right thalamus and the contralateral calcarine sulcus and right cuneus. Furthermore, the neural activation of the left calcarine sulcus was positively correlated with visual analogue scale scores (r = 0.319, p = 0.043), and enhanced FC between the left thalamus and right cuneus in migraine patients was negatively correlated with Generalized Anxiety Disorder scores (r = − 0.617, p = 0.005). Conclusion: Our data suggest that migraine distress is exacerbated by aberrant feedback projections to the visual network, playing a crucial role in migraine physiological mechanisms. The current study provides further insights into the complex scenario of migraine mechanisms.

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Visual input drives increased occipital responsiveness and harmonized oscillations in multiple cortical areas in migraineurs

Cited by 23 publications

References 63 publications

Short-latency afferent inhibition and somato-sensory evoked potentials during the migraine cycle: surrogate markers of a cycling cholinergic thalamo-cortical drive?

Short-latency afferent inhibition and somato-sensory evoked potentials during the migraine cycle: surrogate markers of a cycling cholinergic thalamo-cortical drive?

Cortical Hyper‐Excitability in Migraine in Response to Chromatic Patterns

Impaired intrinsic functional connectivity between the thalamus and visual cortex in migraine without aura

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