Learning-Associated Gamma-Band Phase-Locking of Action–Outcome Selective Neurons in Orbitofrontal Cortex

Abstract

Gamma oscillations (30-100 Hz) correlate to a variety of neural functions, including sensory processing, attention, and action selection. However, they have barely been studied in relation to emotional processing and valuation of sensory signals and actions. We conducted multineuron and local field potential recordings in the orbitofrontal cortex (OFC) of rats performing a task in which they made go or no-go decisions based on two olfactory stimuli predicting appetitive or aversive outcomes. Gamma power was strongest during the late phase of odor sampling, just before go/no-go movement, and increased with behavioral learning. Learning speed was correlated to the slope of the gamma power increment. Spikes of OFC neurons were consistently timed to the gamma rhythm during odor sampling, regardless of the associated outcome. However, only a specific subgroup of cells showed consistent phase timing. These cells showed action-outcome selective activity, not during stimulus sampling but during subsequent movement responses. During sampling, this subgroup displayed a suppression in firing rate but a concurrent increment in the consistency of spike timing relative to gamma oscillations. In addition to gamma rhythm, OFC field potentials were characterized by theta oscillations during odor sampling. Neurons phase-locked to either theta or gamma rhythms but not to both, suggesting that they become associated with separate rhythmic networks involving OFC. Altogether, these results suggest that OFC gamma-band synchronization reflects inhibitory control over a subpopulation of neurons that express information about the emotional valence of actions after a motor decision, which suggests a novel mechanism for response inhibition.