GAMMA-PHASE RELATIONS BETWEEN NEURONS DETERMINE THE EFFECTIVENESS OF INFORMATION ROUTING, PROCESSING, AND BEHAVIOR IN THE VISUAL CORTEX

Flexible, goal-directed behavior requires selective routing and processing of relevant information while suppressing competing inputs. Phase synchronization of rhythmic neuronal activity has been proposed as a mechanism underlying this selection. This mechanism predicts that the timing of synaptic input relative to the receiver neuron’s γ-oscillatory cycle determines effective connectivity: input arriving during γ-phases of high excitability has a greater impact, whereas input arriving during other phases has a reduced impact. To investigate whether precise γ-phase synchronization between neurons processing task-relevant information causally determines effective information routing and processing, we recorded neuronal activity in visual cortical areas of two rhesus monkeys during a demanding shape-tracking task. While the animals performed the task, intracortical microstimulation (ICM) was applied to area V2 to assess whether the impact of ICM-evoked spikes on downstream V4 neurons and behavior varied with the ongoing γ-phase in V4. Moreover, we analyzed whether stimulus information routing between granular and supragranular layers of V1 depended on precise γ-phase synchronization between these populations. The effectiveness of ICM in eliciting spikes in V4-neurons and influencing behavior varied systematically with the ongoing γ-phase of V4-neurons, demonstrating the causal relevance of precise sender–receiver phase relations for effective information routing. Furthermore, stimulus information routing was enhanced during sustained periods of optimal γ-phase alignment, whereas stable but non-optimal phase relations were associated with substantially reduced information transfer. These findings demonstrate that γ-phase relations determine the effectiveness of interareal and interlaminar signal routing and constitute a powerful gating mechanism required for goal-directed behavior.