Hexagonal modulation of theta rhythmic attentional sampling of visual space

Spatial attention improves visual perception by selecting behaviorally relevant sensory signals. Traditionally, attention has been conceptualized as a static spotlight, while recent evidence posited that attention operates as a moving spotlight that samples visual space sequentially in discrete snapshots that are clocked by theta rhythms (∼3-8 Hz). While theta rhythmic attentional sampling has mainly been observed in fronto-parietal and occipital areas, theta oscillations also hallmark entorhinal-hippocampal grid-cell networks, which encode physical space in hexagonal patterns that guide overt exploration and navigation. We hypothesized that visual attention might rely on the same underlying principles and sample visual space in a hexagonal, grid-like configuration. To test this hypothesis, twenty participants (10 females and 10 males) performed a cue-guided attention task that probed behavioral performance as a function of space and time. Reaction times were assessed as a function of spatial location and varying cue-target intervals, which displayed spatially-structured theta rhythms. Specifically, higher theta power occurred at spatial locations that were aligned to multiples of 60°, consistent with an underlying hexagonal organization. Participants that exhibited stronger hexagonal sampling relied less on the spatial cue to guide their attentional allocation. In sum, these findings suggest that covert visual attention is organized in a hexagonal pattern that might be consistent with the grid-like structure known from the entorhinal-hippocampal system and highlight that theta rhythms could reflect a common organizing principle for spatial cognition. Significance Statement Attention prioritizes sensory inputs to optimize behavior. But how does attention sample the environment in space and time? Here, we demonstrate that attentional sampling of visual space is not uniform, but might preferentially explore locations that are oriented along a hexagonal pattern, reminiscent of the spatial configuration of entorhinal-hippocampal grid cells. Moreover, covert attentional sampling exhibited oscillatory theta signatures (3-8 Hz). In sum, these findings suggest that spatial attention and navigation may share a common organizing principle, and indicate that theta rhythms may orchestrate sampling behaviors in space and time as a unifying principle underlying spatial cognition.