Burst Firing Synchronizes Prefrontal and Anterior Cingulate Cortex during Attentional Control

Abstract

Background It is widely held that single cells in anterior cingulate and lateral prefrontal cortex (ACC/PFC) coordinate their activity during attentional processes, although cellular activity that may underlie such coordination across ACC/PFC has not been identified. We thus recorded cells in five ACC/PFC subfields of macaques engaged in a selective attention task, characterized those spiking events that indexed attention, and identified how spiking of distinct cell populations synchronized between brain areas.Results We found that cells in ACC/PFC increased the firing of brief 200 Hz spike bursts when subjects shifted attention and engaged in selective visual processing. In contrast to nonburst spikes, burst spikes synchronized over large distances to local field potentials at narrow beta (12-20 Hz) and at gamma (50-75 Hz) frequencies. Long-range burst synchronization was anatomically specific, functionally connecting those subfields in area 24 (ACC) and area 46 (PFC) that are key players of attentional control. By splitting cells into putative excitatory (pE) and inhibitory (pI) cells by their broad and narrow spikes, we identified that bursts of pI cells preceded and that bursts of pE cells followed in time periods of maximal beta coherent network activity. In contrast, gamma bursts were transient impulses with equal timing across cell classes.Conclusions These findings suggest that processes underlying burst firing and burst synchronization are candidate mechanisms to coordinate attention information across brain areas. We speculate that distinct burst-firing motifs realize beta and gamma synchrony to trigger versus maintain functional network states during goal-directed behavior.