Phase of Firing Coding of Learning Variables across Prefrontal Cortex, Anterior Cingulate Cortex and Striatum during Feature Learning

Abstract The prefrontal cortex and striatum form a recurrent network whose spiking activity encodes multiple types of learning-relevant information. This spike-encoded information is evident in average firing rates, but finer temporal coding might allow multiplexing and enhanced readout across the connected the network. We tested this hypothesis in the fronto-striatal network of nonhuman primates during reversal learning of feature values. We found that neurons encoding current choice outcomes, outcome prediction errors, and outcome history in their firing rates also carried significant information in their phase-of-firing at a 10-25 Hz beta frequency at which they synchronized across lateral prefrontal cortex, anterior cingulate cortex and striatum. The phase-of-firing code exceeded information that could be obtained from firing rates alone, was strong for inter-areal connections, and multiplexed information at three different phases of the beta cycle that were offset from the preferred spiking phase of neurons. Taken together, these findings document the multiplexing of three different types of information in the phase-of-firing at an interareally shared beta oscillation frequency during goal-directed behavior. Highlights Lateral prefrontal cortex, anterior cingulate cortex and striatum show phase-of-firing encoding for outcome, outcome history and reward prediction errors. Neurons with phase-of-firing code synchronize long-range at 10-25 Hz. Spike phases encoding reward prediction errors deviate from preferred synchronization phases. Anterior cingulate cortex neurons show strongest long-range effects.