Experience Reorganizes Coordinated Population Dynamics Across Hippocampal Circuits

Abstract

Hippocampal function relies on structured patterns of population activity that reflect the intrinsic organization of the circuit. Although experience is known to influence synaptic properties and local activity features, whether prolonged experience reshapes the large-scale organization of population dynamics across hippocampal subfields in the intact brain has remained unclear. Progress on this question has been limited by the lack of measurements that capture circuit-wide activity simultaneously while preserving spatial circuit structure. Here, we combined prolonged environmental experience with large-scale, simultaneous multi-shank recordings spanning CA1, CA3, and dentate gyrus in the mouse hippocampus to examine experience-dependent changes in circuit dynamics. We find that long-term experience reorganizes the basal operating state of the hippocampus, altering the statistical structure of field potentials, population spiking, and sharp-wave ripple activity in a coordinated manner across subfields. These changes are not confined to specific regions but instead reflect a circuit-wide reconfiguration of functional interactions that extends over larger spatial scales. At the population level, experience shifts hippocampal dynamics into a more coordinated dynamical regime, characterized by shared low-dimensional structure across hippocampal subfields. Together, these findings demonstrate that long-term experience reorganizes coordinated population dynamics across hippocampal circuits, establishing an intrinsic activity organization that reflects the experiential history of a memory network.