Two Oscillatory Correlates of Attention Control in the Alpha-Band with Distinct Consequences on Perceptual Gain and Metacognition

Abstract

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 with a noninformative cue. Lateralized α amplitude modulation during visuospatial attention shifts has been suggested to account for such perceptual gain. However, recent studies on spontaneous fluctuations of prestimulus α amplitude have challenged this notion. These studies showed that spontaneous fluctuations of prestimulus α amplitude were associated with the subjective appreciation of stimulus occurrence, while objective accuracy was instead best predicted by the frequency of α oscillations, with faster prestimulus α 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 α amplitude but also α frequency in a retinotopic manner. Behaviorally, the cue significantly impacted subjective performance measures (metacognitive abilities [meta-d′]) and objective performance gain (d′). Importantly, α amplitude directly accounted for confidence levels, with ipsilateral synchronization and contralateral desynchronization coding for high-confidence responses. Crucially, the contralateral α amplitude selectively predicted interindividual 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 α 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 STATEMENTPrior 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 α amplitude modulations and reflecting internal decision processes, associated with subjective perceptual experience and metacognitive abilities; the other relying on α 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.