Two oscillatory correlates of attention control in the alpha-band with distinct consequences on perceptual gain and metacognition.

Behavioral consequences and neural underpinnings of visuospatial attention have long been investigated. Classical studies using the Posner paradigm have found that visual perception systematically benefits from the use of a spatially informative cue pointing to the to-be-attended spatial location, compared to a non-informative cue. Lateralized alpha-amplitude modulation during visuospatial attention shifts has been suggested to account for such perceptual gain. However, recent studies on spontaneous fluctuations of prestimulus alpha-amplitude have challenged this notion. These studies showed that spontaneous fluctuations of prestimulus alpha-amplitude were associated with the subjective appreciation of stimulus occurrence, while objective accuracy was instead best predicted by the frequency of alpha oscillations, with faster prestimulus alpha-frequency accounting for better perceptual performance. Here, in male and female humans, by using an informative cue in anticipation of lateralized stimulus presentation, we found that the predictive cue not only modulates preparatory alpha-amplitude but also alpha-frequency in a retinotopic manner. Behaviorally, the cue significantly impacted subjective performance measures (metacognitive abilities, namely meta-d') and objective performance gain (d'). Importantly, alpha-amplitude directly accounted for confidence levels, with ipsilateral synchronization and contralateral desynchronization coding for high-confidence responses. Crucially, the contralateral alpha-amplitude selectively predicted inter-individual differences in metacognitive abilities (meta-d'), thus anticipating decision strategy and not perceptual sensitivity, probably via excitability modulations. Instead, higher perceptual accuracy both within and across participants (d') was associated with faster contralateral alpha-frequency, likely by implementing higher sampling at the attended location. These findings provide critical new insights into the neural mechanisms of attention control and its perceptual consequences. SIGNIFICANCE STATEMENT: Prior knowledge serves the anticipation of sensory input to reduce sensory ambiguity. The growing interest in the neural mechanisms governing the integration of sensory input into our internal representations has highlighted a pivotal role of brain oscillations. Here we show that distinct but interacting oscillatory mechanisms are engaged during attentional deployment: one relying on alpha-amplitude modulations and reflecting internal decision processes, associated with subjective perceptual experience and metacognitive abilities; the other relying on alpha-frequency modulations and enabling mechanistic sampling of the sensory input at the attended location to influence objective performance. These insights are crucial for understanding how we reduce sensory ambiguity to maximize the efficiency of our conscious experience, but also in interpreting the mechanisms of atypical perceptual experiences.