Distributed attention is implemented through theta-rhythmic gamma modulation

Abstract

When subjects monitor a single spatial location, target detection depends on the pre-target phase of an ~8 Hz brain rhythm. When multiple locations are monitored, performance decrements suggest a division of the 8 Hz rhythm over the number of locations. This suggests that different locations are sequentially sampled. Indeed, when subjects monitor two locations, performance benefits alternate at a 4 Hz rhythm. These performance alternations followed a reset of attention to one location. Although resets are common and important events for attention, it is unknown, whether in the absence of resets, ongoing attention operates rhythmically. Here, we examined whether spatially specific attentional sampling can be revealed by ongoing pre-target brain rhythms. Specifically, visually induced gamma-band activity plays a role in spatial attention and therefore, we hypothesized that performance can be predicted by a theta-rhythmic gamma modulation. Brain rhythms were assessed with MEG, while subjects monitored bilateral grating stimuli for a unilateral target. The corresponding contralateral gamma-band responses were subtracted from each other to isolate spatially-selective, target-related fluctuations. The resulting lateralized-gamma activity (LGA) showed opposite 4 Hz phases prior to detected versus missed targets. The 4 Hz phase of pre-target LGA accounted for a 14% modulation in performance. These findings suggest that spatial attention is an ongoing theta-rhythmic sampling process, with each sampling cycle implemented through gamma-band synchrony. This extends previous findings by demonstrating that in the case of distributed attention, gamma-band synchrony is shaped by the slower sampling rhythm that governs performance benefits.