Cortical oscillatory dysrhythmias in visual snow syndrome: a magnetoencephalography study

Abstract

Visual snow refers to the persistent visual experience of static in the whole visual field of both eyes. It is often reported by patients with migraine and co-occurs with conditions such as tinnitus and tremor. The underlying pathophysiology of the condition is poorly understood. Previously, we hypothesized that visual snow syndrome may be characterized by disruptions to rhythmical activity within the visual system. To test this, data from 18 patients diagnosed with visual snow syndrome, and 16 matched controls, were acquired using magnetoencephalography. Participants were presented with visual grating stimuli, known to elicit decreases in alpha-band (8-13 Hz) power and increases in gamma-band power (40-70 Hz). Data were mapped to source-space using a beamformer. Across both groups, decreased alpha power and increased gamma power localized to early visual cortex. Data from the primary visual cortex were compared between groups. No differences were found in either alpha or gamma peak frequency or the magnitude of alpha power, p > 0.05. However, compared with controls, our visual snow syndrome cohort displayed significantly increased primary visual cortex gamma power, p = 0.035. This new electromagnetic finding concurs with previous functional MRI and PET findings, suggesting that in visual snow syndrome, the visual cortex is hyperexcitable. The coupling of alpha-phase to gamma amplitude within the primary visual cortex was also quantified. Compared with controls, the visual snow syndrome group had significantly reduced alpha-gamma phase-amplitude coupling, p < 0.05, indicating a potential excitation-inhibition imbalance in visual snow syndrome, as well as a potential disruption to top-down 'noise-cancellation' mechanisms. Overall, these results suggest that rhythmical brain activity in the primary visual cortex is both hyperexcitable and disorganized in visual snow syndrome, consistent with this being a condition of thalamocortical dysrhythmia.

Keywords: dysrhythmia; magnetoencephalography; migraine; phase–amplitude coupling; visual snow.

Graphical Abstract

Figure 1

Experimental paradigm. Following a 2.0, 3.0 or 4.0 s baseline period, participants were presented with a visual grating (1.5 s duration). A cartoon alien or astronaut picture (duration 1.0 s) was then presented. The subsequent presentation of a ‘?’ symbol was the imperative signal for a response to an alien (response time up to 1.0 s). Participants were instructed to provide no response to astronauts. The alien/astronaut stimuli were to maintain attention and were not part of the analysed data.

Figure 2

Whole-brain representation. Following visual grating presentation, the change (dB) in gamma power (40–70 Hz; 0.3–1.5 s, upper panel) and alpha power (8–13 Hz, 0.3–1.5 s, lower panel) were calculated across a whole-brain grid. Results for the control group (left) and VSS group (right) were averaged and interpolated onto a 3D cortical mesh and finally thresholded at values >1.3 dB (gamma) and less than −0.3 dB (alpha) for illustrative purposes.

Figure 3

V1 power and peak frequency. For both control and VSS groups, violin plots were produced (with median and interquartile range lines) to show: (A) V1 gamma power; (B) V1 peak frequency; (C) V1 alpha power; (D) V1 alpha peak frequency. Dots correspond to data from individual participants. Group differences were analysed using an independent samples t-test, two-tailed.

Figure 4

V1 phase–amplitude coupling. The control group (left panel) showed increased alpha–gamma PAC compared with baseline, with a peak between 50–80 Hz amplitude and 8–9 Hz phase. The VSS group (middle panel) showed less prominent increases in PAC across the comodulogram. Non-parametric statistical comparison (see the Material and methods) indicated significantly greater PAC for the control compared to the VSS group (p < 0.05) from 54 to 76 Hz amplitude and 8 to 9 Hz phase (right panel).