Theta gates and routes information in the frontal cortex

Theta (4-10 Hz) oscillations seem well-suited for coordinating neural activity. Many studies have focused on theta's role in long-range coordination across brain regions (e.g., connectivity between the prefrontal cortex and the hippocampus). It remains unclear how theta coordinates neural activity more locally within prefrontal subareas. We examined neural activity in three frontal areas (i.e., dorsolateral prefrontal cortex (dlPFC), ventrolateral prefrontal cortex (vlPFC), and frontal eye fields (FEF)) as non-human primates categorized dot patterns. We found that theta flexibly coordinated spiking activity and higher-frequency oscillations within and between frontal areas. First, theta phase in all areas was coupled to spiking information in the FEF and seemed to gate information that was behaviorally relevant. Second, theta influences were routed in opposite directions depending on feedback. Theta flowed in a posterior direction to the FEF during choices and after correct outcomes. Theta influences reversed directionality and flowed in an anterior direction after incorrect outcomes. Third, theta organized nested cross-frequency, phase-amplitude interactions. Theta was coupled to beta (15-30Hz) oscillations, both within and between areas. Beta, in turn, was coupled to gamma (40-90Hz) oscillations, but mainly locally. Together, our results position theta as a critical mechanism that flexibly and dynamically coordinates neural activity within and across the frontal cortex.