Alpha phase-amplitude tradeoffs predict visual perception

Spontaneous alpha oscillations (~10 Hz) have been associated with various cognitive functions, including perception. Their phase and amplitude independently predict cortical excitability and subsequent perceptual performance. Yet, the causal role of alpha 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 alpha oscillations are associated with periodic functional inhibition. (1) High alpha 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 alpha 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 post-pulse evoked activity recorded with simultaneous electroencephalography (EEG). We observed that pre-pulse alpha phase modulates the probability to perceive a phosphene, predominantly for high alpha amplitude, with a non-optimal phase for phosphene perception between -{pi}/2 and -{pi}/4. The pre-pulse non-optimal phase further leads to an increase in post-pulse evoked activity (ERP), in phosphene-perceived trials specifically. Together, these results show that alpha oscillations create periodic inhibitory moments when alpha amplitude is high, leading to periodic decrease of perceptual performance. This study provides strong causal evidence in favor of the Pulsed Inhibition theory. Visual Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=83 SRC="FIGDIR/small/445552v3_ufig1.gif" ALT="Figure 1"> View larger version (16K): org.highwire.dtl.DTLVardef@1c6e4f8org.highwire.dtl.DTLVardef@e26614org.highwire.dtl.DTLVardef@19bc93forg.highwire.dtl.DTLVardef@b97b36_HPS_FORMAT_FIGEXP M_FIG C_FIG Significance StatementThe Pulsed Inhibition theory predicts that the functional inhibition induced by high alpha oscillations amplitude is periodic, with specific phases decreasing neural firing and perceptual performance. In turn, low alpha oscillations amplitude is less susceptible to phasic moments of pulsed inhibition leading to overall higher perceptual performance. Using TMS with simultaneous EEG recordings in humans, we found that specific phases of spontaneous alpha oscillations (~10 Hz) decrease cortical excitability and the subsequent perceptual outcomes predominantly when alpha amplitude is high. Our results provide strong causal evidence in favor of the Pulsed Inhibition theory.