α Phase-Amplitude Tradeoffs Predict Visual Perception

Abstract

Spontaneous α oscillations (∼10 Hz) have been associated with various cognitive functions, including perception. Their phase and amplitude independently predict cortical excitability and subsequent perceptual performance. However, the causal role of α phase-amplitude tradeoffs on visual perception remains ill-defined. We aimed to fill this gap and tested two clear predictions from the pulsed inhibition theory according to which α oscillations are associated with periodic functional inhibition. (1) High-α amplitude induces cortical inhibition at specific phases, associated with low perceptual performance, while at opposite phases, inhibition decreases (potentially increasing excitation) and perceptual performance increases. (2) Low-α amplitude is less susceptible to these phasic (periodic) pulses of inhibition, leading to overall higher perceptual performance. Here, cortical excitability was assessed in humans using phosphene (illusory) perception induced by single pulses of transcranial magnetic stimulation (TMS) applied over visual cortex at perceptual threshold, and its postpulse evoked activity recorded with simultaneous electroencephalography (EEG). We observed that prepulse α phase modulates the probability to perceive a phosphene, predominantly for high-α amplitude, with a nonoptimal phase for phosphene perception between –π/2 and –π/4. The prepulse nonoptimal phase further leads to an increase in postpulse-evoked activity [event-related potential (ERP)], in phosphene-perceived trials specifically. Together, these results show that α oscillations create periodic inhibitory moments when α amplitude is high, leading to periodic decrease of perceptual performance. This study provides strong causal evidence in favor of the pulsed inhibition theory.

Significance Statement

The pulsed inhibition theory predicts that the functional inhibition induced by high-α oscillations’ amplitude is periodic, with specific phases decreasing neural firing and perceptual performance. In turn, low-α oscillations’ amplitude is less susceptible to phasic moments of pulsed inhibition leading to overall higher perceptual performance. Using transcranial magnetic stimulation (TMS) with simultaneous electroencephalography (EEG) recordings in humans, we found that specific phases of spontaneous α oscillations (∼10 Hz) decrease cortical excitability and the subsequent perceptual outcomes predominantly when α amplitude is high. Our results provide strong causal evidence in favor of the pulsed inhibition theory.