Cross-frequency coordination in a hippocampo-cortical circuit during probabilistic reversal learning.

Learning under uncertainty requires detecting latent changes in environmental contingencies and flexibly adjusting choice strategy. To examine hippocampo-cortical circuit dynamics during probabilistic choice behavior, we trained rats on a two-armed bandit task with uncued reward reversals while recording local field potentials from dorsal hippocampus (CA1d), lateral entorhinal cortex (LEC), and prefrontal cortex (PFC). Performance improved across sessions, shifting from outcome-reactive exploration to exploitation, quantified using a model-free index. Mixed-effects modeling identified session-averaged cortical synchrony in theta and fast-gamma bands as a negative performance marker. Theta and gamma oscillations were coordinated, with CA1d theta coupled with fast-gamma in PFC, and modulated slow- and fast-gamma bursts in LEC, selectively increasing at goal-reaching. Neuronal spiking showed pathway-specific phase-locking, with theta-dependent spike timing across hippocampo-cortical pairs and reciprocal slow-gamma phase-locking most evident between CA1d and LEC. Distributed spiking was modulated during goal approach, with sustained peri-goal ramping in PFC putative single units, whereas hippocampal and entorhinal populations showed transient suppression around nosepoke onset. These results identify a session-averaged LEC-PFC connectivity marker of task performance and dissociate it from hippocampal theta mechanisms organizing cortical gamma bursts and spike timing during peri-goal processing, providing a circuit-level framework for adaptive decision-making under uncertainty.