Neuronal information processing causally depends on gamma phase synchrony

Abstract

Abstract Successful behaviour relies on the brain’s ability to flexibly process relevant information while suppressing irrelevant information1. Visual neurons show functional flexibility by selectively responding to subsets of inputs representing attended objects while ignoring those conveying information about irrelevant objects2–5. Several neuronal mechanisms underlying such attention-dependent processing have been proposed. However, causation has not yet been proven6–9. We show that the spike arrival time with respect to the receiving neurons’ γ-oscillatory activity is causal to the spikes’ impact on these neurons and behaviour. We performed intracortical microstimulation (ICM) in area V2 of macaque monkeys to evoke spikes. These ICM-evoked spikes caused a significant increase in the spiking activity of receiving V4 neurons and a significant delay in monkeys’ responses. These effects were observed only when ICM-evoked spikes arrived close to the peak of the neurons’ excitability cycle, with no effects observed during other phases of the V4 γ-cycle. Our results demonstrate that phase synchronization between input spikes and receiver neurons is causal for selective signal routing and required for flexible network configuration. These results are significant for future theoretical and experimental research on selective information processing and brain-computer interfaces.