Phase shifts in high-beta- and low-gamma-band local field potentials predict the focus of visual spatial attention

Abstract

The local field potential (LFP) contains rich information about activity in local neuronal populations. However, it has been challenging to establish direct links between LFP modulations and task-relevant behavior or cognitive processes, such as attention. We sought to determine whether LFP amplitude or phase modulations are predictive of the allocation of visual spatial attention. LFPs were recorded simultaneously in multiple early visual brain structures of alert macaque monkeys performing attention-demanding detection and discrimination tasks. Attention directed toward the receptive field of recorded neurons generated systematically larger phase shifts in high-beta- and low-gamma-frequency LFPs compared with LFP phase shifts on trials in which attention was directed away from the receptive field. This attention-mediated temporal advance corresponded to ~10 ms. LFP phase shifts also correlated with reaction times when monkeys were engaged in the tasks. Importantly, attentional modulation of LFP phase was consistent across monkeys, tasks, visual brain structures, and cortical layers. In contrast, attentional modulation of LFP amplitude varied across frequency bands, visual structures/layers, and tasks. Because LFP phase shifts were robust, consistent, and predictive of spatial attention, they could serve as a reliable marker for attention signals in the brain. NEW & NOTEWORTHY Local field potentials (LFPs) reflect the activity of spatially localized populations of neurons. Whether alterations in LFP activity are indicative of cognitive processes, such as attention, is unclear. We found that shifts in the phase of LFPs measured in multiple visual brain areas reliably predicted the focus of spatial attention. LFP phase shifts could therefore serve as a marker for behaviorally relevant attention signals in the brain.