Population-Level Activity Dissociates Preparatory Overt from Covert Attention

The neural signatures of preparing overt eye movements and directing covert spatial attention overlap as they recruit the same brain areas. Yet, these neural signatures are dissociable at the single-cell level: Specific cells within visuo-oculomotor areas are exclusively involved in motor preparation or covert attention. Nevertheless, it has been proposed that many cells in visuo-oculomotor areas are involved in both motor preparation and covert attention, and consequently their neural signatures should functionally overlap to a large degree. Here, we directly tested this proposal: we combined human (both sexes) EEG with sensitive decoding techniques to investigate whether the neural signatures of preparatory overt and covert attention are dissociable across large-scale neuronal populations. We found that neural decoding reliably discerned whether overt or covert attention was shifted well before saccade initiation. Further, inverted encoding modeling revealed earlier and sharper spatially-tuned activity in preparatory overt than in covert attention. We then asked whether preparatory overt attention achieved sharper spatially-tuned activity by using ‘more-of-the-same’ covert attention, or by recruiting additional spatially selective neural processing. Cross-decoding results demonstrated that preparatory overt attention recruited at least one additional, frontal process. This additional spatially selective process emerged early and likely reflects motor preparation or predictive remapping. To summarize, we found that the neural signatures of overt and covert attention overlap, yet diverge rapidly, in part because overt attention employs an additional spatially selective neural process. Extending beyond a dissociation on the single-cell level, our findings demonstrate that population-level neural activity dissociates preparatory overt from covert attention. Significance statement The world provides much more visual input than the brain can process simultaneously. Spatial visual attention allows for the selective processing of only the most important parts of this input. Spatial attention shifts either overtly (with an eye movement) or covertly (without an accompanying eye movement). The neural signatures underlying these types of spatial attention have long thought to overlap to a large degree. This strong overlap was thought to only break down at the level of single neurons. In our EEG study, we instead demonstrate that large populations of neurons dissociate overt from covert attention. Our results show that the neural signatures of overt and covert attention differ on a much broader scale than previously thought.