Hippocampal consummatory reward ensembles dynamically engage theta-SWR states during spatial working memory

Abstract

Reward consumption consists of temporally structured sensory and behavioral episodes critical for memory-guided behavior. However, how hippocampal circuits organize consummatory episodes and their associated oscillatory activity remains poorly understood. Recording dorsal hippocampal CA1 activity during a delayed nonmatch-to-place T-maze task, we identified a sparse population of reward-ensemble neurons with sustained firing aligned to distinct phases of reward consumption and spatially centered on reward locations. Reward consumption was accompanied by chewing-linked, atropine-sensitive 6-Hz theta oscillations that coexisted with intermittent sharp-wave ripples (SWRs). Notably, coupling of reward-ensemble spiking to theta and SWRs differed across sample and test phases of the task, suggesting state-dependent coordination of hippocampal reward ensembles during spatial working memory. Together, these findings identify reward consumption as a distinct hippocampal state characterized by coordinated theta-SWR dynamics during mnemonic behavior.