Hexagonal modulation of theta rhythmic attentional sampling of visual space

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Abstract

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 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 revealed prominent, spatially-structured theta rhythms. Specifically, higher theta power was evident 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 relies on an underlying hexagonal grid-like structure known from the entorhinal-hippocampal system and highlight that theta rhythms 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 preferentially explores locations that are oriented along a hexagonal pattern, reminiscent of the spatial configuration of entorhinal-hippocampal grid cells. Moreover, covert attentional sampling was clocked by theta oscillations (3-8 Hz). In sum, these findings provide evidence for a shared neural basis of underlying spatial attention and navigation and reveal that theta rhythms orchestrate sampling behaviors in space and time as a unifying principle underlying spatial cognition.

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