Distinct theta mechanisms mediate target enhancement and distractor suppression in the primate prefrontal--V4 network

Selective attention necessitates amplifying salient stimuli while extinguishing irrelevant inputs. The prefrontal cortex (PFC) is believed to orchestrate both mechanisms through top-down regulation of visual cortex, yet the shared versus separate nature of facilitation and suppression within the prefrontal--visual network remains unclear.

Simultaneous recordings of neuronal activity and local field potentials were obtained from the PFC and visual area V4 as monkeys executed a covert spatial attention task. PFC exhibited earlier manifestation of spatial attention signals compared to V4, with target location information conveyed from PFC to V4, while target identity was conveyed from V4 to PFC subsequent to target selection.

Notably, theta band oscillations assumed distinct roles at each stage. Target selection correlated with heightened PFC theta activity and augmented PFC-to-V4 theta connectivity, which preceded heightened V4 gamma activity and V4-to-PFC gamma influences. Conversely, when the same stimulus functioned as a distractor, PFC theta input to the corresponding V4 population was diminished or absent.

Instead, the distractor-encoding V4 population displayed augmented local theta activity, a consistent modification in theta phase, and stronger theta-gamma phase-amplitude coupling. Within V4, heightened theta-gamma coupling constrained gamma activity to specific phases of the theta cycle and predicted behavior for both targets and distractors in opposing manners.

These findings elucidate a division of labor within the prefrontal--visual network: PFC instigates target selection via theta-band signaling to V4, whereas distractor suppression emerges locally within V4 through theta-dependent gamma gating.