Distributed Attention Is Implemented through Theta-Rhythmic Gamma Modulation

Highlights

• Two stimuli’s gamma responses are subtracted (LGA) to reveal attentional biases

• The 4 Hz phase of LGA before one of the stimuli dims predicts detection accuracy

• The magnitude of this accuracy modulation is 14.5% of the average accuracy

• The 4 Hz modulation of gamma responses was evident throughout the attention period

Summary

When subjects monitor a single location, visual target detection depends on the pre-target phase of an ∼8 Hz brain rhythm [1, 2]. When multiple locations are monitored, performance decrements suggest a division of the 8 Hz rhythm over the number of locations [3], indicating that different locations are sequentially sampled. Indeed, when subjects monitor two locations, performance benefits alternate at a 4 Hz rhythm [4]. These performance alternations were revealed after a reset of attention to one location. Although resets are common and important events for attention [5], it is unknown whether, in the absence of resets, ongoing attention samples stimuli in alternation. Here, we examined whether spatially specific attentional sampling can be revealed by ongoing pre-target brain rhythms. Visually induced gamma-band activity plays a role in spatial attention. Therefore, we hypothesized that performance on two simultaneously monitored stimuli can be predicted by a 4 Hz modulation of gamma-band activity. Brain rhythms were assessed with magnetoencephalography (MEG) while subjects monitored bilateral grating stimuli for a unilateral target event. The corresponding contralateral gamma-band responses were subtracted from each other to isolate spatially selective, target-related fluctuations. The resulting lateralized gamma-band activity (LGA) showed opposite pre-target 4 Hz phases for detected versus missed targets. The 4 Hz phase of pre-target LGA accounted for a 14.5% modulation in performance. These findings suggest that spatial attention is a theta-rhythmic sampling process that is continuously ongoing, with each sampling cycle being implemented through gamma-band synchrony.