Abstract
Recent behavioral studies suggest that attention samples space rhythmically (1–4). Oscillations in brain activity have been described as a possible mechanism supporting attentional processes (5, 6). However, the precise mechanism through which this rhythmic exploration of space is subserved by the prefrontal cortical regions at the source of attention control signals remains unknown. Here, we apply machine learning methods to ongoing monkey prefrontal multi-unit population activity, to decode in real-time the (x,y) location of the covert attentional spotlight (7), aka the mind’s eye. We demonstrate that this prefrontal attentional spotlight continuously explores space at an alpha 7-12 Hz rate. These oscillations determine both neuronal sensory processing, defining how much information is available in the prefrontal cortex about incoming sensory stimuli, and perception, determining whether these incoming sensory stimuli are prone to elicit an overt behavioral response or not. As a result, when sensory events are presented at a specific optimal phase with respect to these oscillations, sensory encoding is reliable and behavior is accurate. When sensory events are presented in anti-phase with respect to this optimal phase, both sensory encoding and behavioral performance are poor. We propose that this rhythmic prefrontal attentional spotlight activity can be viewed as a continuous exploration of space via alpha-clocked attentional saccades. We demonstrate that these attentional saccades are highly flexible, their pattern of space exploration depending both on within-trial and across-task contingencies. These results are discussed in the context of exploration and exploitation strategies and prefrontal top-down attentional control.
Highlights
The decoded prefrontal attentional spotlight samples visual space in rhythmic cycles
This rhythmic attentional exploration predicts neuronal sensory processing accuracy
This rhythmic attentional exploration predicts overt behavioral accuracy
These rhythmic cycles define alpha-clocked attentional saccades
Space exploration by attentional saccades is highly flexible and under top-down control