Differential neural mechanisms underlie cortical gating of visual spatial attention mediated by alpha-band oscillations

Abstract

ABSTRACTSelective attention relies on neural mechanisms that facilitate processing of behaviorally relevant sensory information while suppressing irrelevant information, consistently linked to alpha-band oscillations in human M/EEG studies. We analyzed cortical alpha responses from intracranial electrodes implanted in eight epilepsy patients, who performed a visual spatial attention task. Electrocorticographic data revealed a spatiotemporal dissociation between attention-modulated alpha desynchronization, associated with the enhancement of sensory processing, and alpha synchronization, associated with the suppression of sensory processing, during the cue-target interval. Dorsal intraparietal areas contralateral to the attended hemifield primarily exhibited a delayed and sustained alpha desynchronization, while ventrolateral extrastriatal areas ipsilateral to the attended hemifield primarily exhibited an earlier and sustained alpha synchronization. Analyses of cross-frequency coupling between alpha phase and broadband high-frequency activity (HFA) further revealed cross-frequency interactions along the visual hierarchy contralateral to the attended locations. Directionality analyses indicate that alpha phase in early and extrastriatal visual areas modulated HFA power in downstream visual areas, thus potentially facilitating the feedforward processing of an upcoming, spatially predictable target. In contrast, in areas ipsilateral to the attended locations, HFA power modulated local alpha phase in early and extrastriatal visual areas, with suppressed interareal interactions, potentially attenuating the processing of distractors. Our findings reveal divergent alpha-mediated neural mechanisms underlying target enhancement and distractor suppression during the deployment of spatial attention, reflecting enhanced functional connectivity at attended locations, while suppressed functional connectivity at unattended locations. The collective dynamics of these alpha-mediated neural mechanisms play complementary roles in the efficient gating of sensory information.SIGNIFICANCE STATEMENTSelective attention relies on neural mechanisms involved in target enhancement and distractor suppression to guide behavior. Using electrocorticographic data in humans, we show a spatiotemporal dissociation between cortical activities engaged in target facilitation and distractor inhibition during attentional deployment. We also found that, at attended locations, interareal interactions are enhanced through cross-frequency coupling along the visual hierarchy to potentially facilitate the processing of a spatially predictable target. In contrast, at unattended locations, intraareal interactions are enhanced through cross-frequency coupling, and interareal interactions are suppressed, together to potentially attenuate the processing of distractors. Our findings reveal that such a distributed cortical organization and complementary neural mechanisms enable efficient gating and filtering of sensory information in the anticipatory processing of spatial attention.