Oscillatory brain activity in the canonical alpha-band conceals distinct mechanisms in attention.

Abstract

Brain oscillations in the alpha-band (8-14Hz) over posterior areas have been linked to specific processes in attention and perception. In particular, decreases in alpha-amplitude are thought to reflect activation of perceptually relevant brain areas for target engagement, while increases in alpha-amplitude have been associated with inhibition for distractor suppression. Traditionally, these alpha-changes have been viewed as two facets of the same process. However, more recent evidence calls for revisiting this interpretation. Here, we concurrently recorded MEG/EEG in 32 participants (19 females) during covert visuo-spatial attention shifts (spatial cues), and two control conditions (neutral cue, no-attention cue), while tracking fixational eye-movements. In disagreement with a single, perceptually relevant alpha-process, we found the typical alpha-modulations contra- and ipsilateral to the attention focus to be triple dissociated in their timing, topography, and spectral features: Ipsilateral alpha-increases occurred early, over occipital sensors, at a high alpha-frequency (10-14Hz) and were expressed during spatial attention (alpha spatial cue > neutral cue). By contrast, contralateral alpha-decreases occurred later, over parietal sensors, at a lower alpha-frequency (7-10Hz) and were associated with attention deployment in general (alpha spatial&neutral cue < no-attention cue). Additionally, the lateralized early alpha-increases but not -decreases during spatial attention coincided in time with directionally biased microsaccades. Overall, these findings suggest that the attention-related early alpha-increases and late -decreases reflect distinct, likely reflexive versus endogenously controlled attention mechanisms. We conclude that there is more than one perceptually relevant posterior alpha-oscillation, which need to be dissociated for a detailed account of their roles in perception and attention.Significance statement This study provides novel insights into perceptually relevant brain oscillations in the "canonical" alpha-band, and the neural correlates of covert and overt attention processes. This by simultaneously recording MEG and EEG, and isolating by design visuospatial and temporal expectations respectively, while tracking fixational eye-movements concurrently to the nominally covert attention shifts. The data reveal the presence of two, spatio-temporally and spectrally dissociated patterns of posterior alpha-changes that are distinctively associated with deployment of spatial and temporal anticipation, and eye-movement activity. This refines our understanding of the role of brain oscillations in perception and attention, the neural underpinnings of attention deployment in space and time, and provides methodological pointers for the study of perceptually relevant oscillatory activity through MEG/EEG.