Theta oscillations in anterior cingulate cortex and orbitofrontal cortex differentially modulate accuracy and speed in flexible reward learning

Flexible reward learning relies on frontal cortex, with substantial evidence indicating the anterior cingulate cortex (ACC) and orbitofrontal cortex (OFC) play important roles. Recent studies in both rat and macaque suggest theta oscillations (5-10 Hz) may be a spectral signature that coordinates this learning. However, causal network-level interactions between ACC and OFC in flexible learning remain unclear. We investigated the learning of stimulus-outcome (S-O) and action-outcome (A-O) associations using a combination of simultaneous in-vivo electrophysiology in dorsal ACC and ventral OFC, partnered with bilateral inhibitory DREADDs in ACC. In freely-behaving male and female rats and using a within-subject design, we examined accuracy and speed of response across distinct and precisely-defined trial epochs including correct choice, incorrect choice, and reward collection. We report significant modulation of accuracy by theta power in both ACC and OFC. Both ACC and OFC theta oscillations consistently signaled accuracy in the initial discrimination phase, whereas it was OFC theta alone in the reversal phases of both S-O and A-O learning. Theta power in either region was not correlated with deliberation speed. Indeed, theta modulation of accuracy was dissociable from its involvement in speed of response which was affected by ACC inhibition, most prominently in A-O learning. Results are discussed with reference to the nonhuman primate literature, where there is by contrast more reported specialization of OFC and ACC in flexible learning of stimuli and actions. The present results also point to a specific role of OFC theta in signaling a reversal of either kind.