Theta-band phase locking of orbitofrontal neurons during reward expectancy

The expectancy of a rewarding outcome following actions and cues is coded by a network of brain structures including the orbitofrontal cortex. Thus far, predicted reward was considered to be coded by time-averaged spike rates of neurons. However, besides firing rate, the precise timing of action potentials in relation to ongoing oscillations in local field potentials is thought to be of importance for effective communication between brain areas. We performed multineuron and field potential recordings in orbitofrontal cortex of rats performing olfactory discrimination learning to study the temporal structure of coding predictive of outcome. After associative learning, field potentials were marked by theta oscillations, both in advance and during delivery of reward. Orbitofrontal neurons, especially those coding information about upcoming reward with their firing rate, phase locked to these oscillations in anticipation of reward. When established associations were reversed, phase locking collapsed in the anticipatory task phase, but returned when reward became predictable again after relearning. Behaviorally, the outcome anticipation phase was marked by licking responses, but the frequency of lick responses was dissociated from the strength of theta-band phase locking. The strength of theta-band phase locking by orbitofrontal neurons robustly follows the dynamics of associative learning as measured by behavior and correlates with the rat's current outcome expectancy. Theta-band phase locking may facilitate communication of outcome-related information between reward-related brain areas and offers a novel mechanism for coding value signals during reinforcement learning.