Phase-precession-like Effects in the Anterior Insula Cortex during Reward Expectancy

Abstract Reward expectancy shapes behavioral performance by coordinating the allocation of cognitive resources, which incorporates the involvement of the anterior insular cortex (AIC). To investigate AIC’s electrophysiological mechanisms during reward expectancy, we collected intracranial electroencephalographic data from epilepsy patients implanted for clinical purposes. During recording, they navigated a virtual T-maze where they encountered rewards at three predetermined locations. We focused on the time window proximal to entering the reward zone, defined as the expectancy stage. During this stage, a robust phase-amplitude coupling (PAC) between theta oscillation and gamma activity was found within the AIC. This PAC exhibited a specific temporal structure, with peak gamma activity progressively coupling to an earlier theta phase before each reward onset. These phase shift phenomena mirrored the phase precession effect, termed phase-precession-like effects (PPLEs). Meanwhile, the reward-specific neural patterns were pre-activated during the expectancy stage of rewards, coinciding with peak gamma activities across trials. Additionally, subjects exhibiting PPLEs in the AIC presented reduced variability and a more pronounced enhancement in response latency across trials. These results revealed potential electrophysiological mechanisms of the AIC underlying reward expectancy.