Pre-Stimulus Alpha-Band Phase Gates Afferent Visual Cortex Responses

Abstract

The neurogenesis of alpha-band (8-13 Hz) activity has been characterized across many different animal experiments. However, the functional role that alpha oscillations play in perception and behavior has largely been attributed to two contrasting hypotheses, with human evidence in favor of either (or both or neither) remaining sparse. On the one hand, alpha generators have been observed in relay sectors of the visual thalamus and are postulated to phasically inhibit afferent visual input in a feedforward manner 1-4. On the other hand, evidence also suggests that the direction of influence of alpha activity propagates backwards along the visual hierarchy, reflecting a feedback influence upon the visual cortex 5-9. The primary source of human evidence regarding the role of alpha phase in visual processing has been on perceptual reports 10-16, which could be modulated either by feedforward or feedback alpha activity. Thus, although these two hypotheses are not mutually exclusive, human evidence clearly supporting either one is lacking. Here, we present human subjects with large, high-contrast visual stimuli that elicit robust C1 event-related potentials (ERP), which peak between 70-80 milliseconds post-stimulus and are thought to reflect afferent primary visual cortex (V1) input 17-20. We find that the phase of ongoing alpha oscillations modulates the global field power (GFP) of the EEG during this first volley of stimulus processing (the C1 time-window). On the standard assumption 21-23 that this early activity reflects postsynaptic potentials being relayed to visual cortex from the thalamus, our results suggest that alpha phase gates visual responses during the first feed-forward sweep of processing.

Alpha Oscillations in Resisting Distraction

“…Other studies failed to find such a link (see below) but a recent attention study provided strong evidence in favor of a link between alpha increase and distractor suppression by showing an inverse relationship between alpha power and the Pd component which indexes distractor interference (Zhao et al, 2023; see also Dou et al, 2021;Iemi et al, 2019).…”

“…A large body of literature shows that the magnitude (and phase) of spontaneous prestimulus alpha oscillations influence visual processing as revealed by stimulus detection measures and event-related potentials (e.g. Iemi et al, 2019;Zazio et al, 2021;Dou et al, 2021;Fakche et al, 2022;VanRullen, 2016). It has therefore been suggested that an alpha power decrease would be associated with an increase sensory excitability, and an alpha power increase would result in a decrease of sensory excitability (see Samaha et al, 2020).…”

“…LGN input. Observing C1 requires to use specific kind of stimuli but a relationship between ongoing alpha power/phase and C1 amplitude has been observed (Dou et al, 2021;Iemi et al, 2019). The optimal way to determine whether alpha oscillations in sensory regions is associated with gain modulation is to use animal recordings (Sellers et al, 2015) which allow to investigate more precisely the link between alpha power and simultaneous excitability or distractor related response.…”