Pop-out search instigates beta-gated feature selectivity enhancement across V4 layers

Visual search is a workhorse for investigating how attention interacts with processing of sensory information. Attentional selection has been linked to altered cortical sensory responses and feature preferences (i.e., tuning). However, attentional modulation of feature selectivity during search is largely unexplored. Here we map the spatiotemporal profile of feature selectivity during singleton search. Monkeys performed a search where a pop-out feature determined the target of attention. We recorded laminar neural responses from visual area V4. We first identified “feature columns” which showed preference for individual colors. In the unattended condition, feature columns were significantly more selective in superficial relative to middle and deep layers. Attending a stimulus increased selectivity in all layers but not equally. Feature selectivity increased most in the deep layers, leading to higher selectivity in extragranular layers as compared to the middle layer. This attention-induced enhancement was rhythmically gated in phase with the beta-band local field potential. Beta power dominated both extragranular laminar compartments, but current source density analysis pointed to an origin in superficial layers, specifically. While beta-band power was present regardless of attentional state, feature selectivity was only gated by beta in the attended condition. Neither the beta oscillation nor its gating of feature selectivity varied with microsaccade production. Importantly, beta modulation of neural activity predicted response times, suggesting a direct link between attentional gating and behavioral output. Together, these findings suggest beta-range synaptic activation in V4’s superficial layers rhythmically gates attentional enhancement of feature tuning in a way that affects the speed of attentional selection.

Throughout cortex, sensory information is organized into maps. This phenomenon is readily observable in visual cortex where maps organize information in both the radial (e.g., within cortical columns) and tangential (e.g., across a cortical area) dimensions (1–4). Importantly, sensory information attributed to these maps is malleable. For example, selective attention is linked to profound changes in neural activity organizing sensory information in both space and time (5–34).In visual cortex, cortical columnar microcircuits comprise many neurons that respond to the same location of visual space and similar stimulus features. For example, primary visual cortex (V1) features “orientation columns” consisting of neurons sharing response preference for the same stimulus orientation (35, 36) and “ocular dominance columns” consisting of neurons that preferentially respond to the same eye (37). Similar columnar organization for feature selectivity has been described across many other visual cortical areas, including area V2 (36, 38, 39), area V3 (40), middle temporal area (area MT) (41–43), and inferotemporal cortex (44–46). Midlevel visual cortical area V4, a well-studied area contributing to attentional modulation, follows suit with columnar organization of visual responses and feature preferences (44, 47–53). Yet, we do not know the extent to which attention impacts feature preferences along columns. While canonical microcircuit models of cortex predict laminar differences for attentional modulation e.g., feedback-recipient extragranular layers modulating before granular layers (54–56)], how this modulation interacts with columnar feature selectivity is largely unknown.We sought to determine the spatiotemporal profile of feature preferences within the V4 laminar microcircuit during attentional selection. To address this question, we performed neurophysiological recordings along V4 layers in monkeys performing an attention-demanding pop-out search task. We identified feature columns demonstrating homogeneous feature preference along cortical depth. When the search array item presented in the column’s receptive field (RF) was unattended, the upper cortical layers were most selective. However, when attended, feature selectivity in the deep layers enhanced the most, resulting in overall strongest feature selectivity in both extragranular compartments. We further found that the enhancement of feature selectivity associated with attention was rhythmically gated in the beta range. While beta activity was measurable across both unattended and attended conditions, rhythmic gating of feature selectivity was only present with attention. Moreover, beta power modulating the neural response was predictive of response time (RT), suggesting a link between attentional gating and behavior. Synaptic currents revealed the beta rhythm originates in superficial cortical layers, which is compatible with top-down influence.