On the role of prestimulus alpha rhythms over occipito-parietal areas in visual input regulation: correlation or causation?

Abstract

The posterior alpha rhythm (8-14 Hz), originating in occipito-parietal areas through thalamocortical generation, displays characteristics of visual activity in anticipation of visual events. Posterior alpha power is influenced by visual spatial attention via top-down control from higher order attention areas such as the frontal eye field. It covaries with visual cortex excitability, as tested through transcranial magnetic stimulation (TMS), and predicts the perceptual fate of a forthcoming visual stimulus. Yet, it is still unknown whether the nature of the relationship between this prestimulus alpha oscillation and upcoming perception is causal or only correlative. Here, we tested in the human brain whether the oscillation in the alpha band is causally shaping perception through directly stimulating visual areas via short trains of rhythmic TMS. We compared stimulation at alpha frequency (10 Hz) with two control frequencies in the theta (5 Hz) and beta bands (20 Hz), and assessed immediate perceptual outcomes. Target visibility was significantly modulated by alpha stimulation, relative to both control conditions. Alpha stimulation selectively impaired visual detection in the visual field opposite to the stimulated hemisphere, while enhancing detection ipsilaterally. These frequency-specific effects were observed both for stimulation over occipital and parietal areas of the left and right hemispheres and were short lived: they were observed by the end of the TMS train but were absent 3 s later. This shows that the posterior alpha rhythm is actively involved in shaping forthcoming perception and, hence, constitutes a substrate rather than a mere correlate of visual input regulation.

Figure 1.

A, Experimental design and task. TMS was applied in trains of five pulses at alpha, theta, or beta frequency (10, 5, or 20 Hz; randomly intermixed) over one of four sites (occipital, parietal × left, right; block design). Real TMS blocks were intermingled with sham blocks (coil perpendicular to the scalp). To assess immediate effects of prestimulus TMS, a near-threshold stimulus was presented simultaneously with the last pulse (0 s) in one of two placeholders, either contralaterally or ipsilaterally to TMS (plus catch trials). To assess offline effects, target visibility was probed for six further time points post-TMS [3, 6, 9, 12, 15, and 18 s (not shown)]. Participants had to respond with the right index finger whenever they perceived a stimulus. The intertrain interval was 22 s. Fixation cross and placeholders stayed continuously on the screen. B, Stimulation sites for one representative participant.

Figure 2.

Frequency- and space-specific biasing of visual detection through rhythmic TMS over occipito-parietal sites for performance at TMS train offset (immediate effects). A, Effects of rhythmic TMS (5, 10, and 20 Hz) on hit rate (sham normalized = real − sham) for target detection ipsilateral (light gray bars) and contralateral to TMS (dark gray bars). Data are collapsed over all four TMS positions (occipital, parietal × left, right), as frequency-specific effects did not interact with either TMS site or TMS side. B, False alarm rate to catch trials, collapsed over all stimulation sites. Asterisks point to significant differences: *p < 0.05; **p < 0.01; ***p < 0.001.

Figure 3.

Effect evolution over the intertrain interval (22 s). The frequency- and space-specific biasing of visual detection through rhythmic TMS is temporally restricted. It is present at train offset (0 s) but disappeared ≥3 s post-train.