Experience-dependent diversification of ripple firing and synaptic inputs in hippocampal CA1

ABSTRACT The hippocampus plays a key role in encoding episodic memory by transforming recent experience into persistent neuronal and synaptic modifications. However, the physiological processes that link real-world experience to coordinated network activity and synaptic reorganization remain incompletely understood. Here, we investigated how distinct types of episodic experience reshape ensemble firing dynamics and synaptic input in the hippocampal CA1 region of freely moving rats. We identified spontaneous super bursts , defined as brief episodes of high-frequency population firing, that emerged preferentially during emotionally salient experiences. These bursts were associated with an increase in ripple firing, defined as short-duration, high-frequency multi-unit spike activity occurring in association with sharp-wave ripples. Analysis of ripple firing patterns revealed experience-dependent diversification, reflected by increased information entropy after episodic experience. Ex vivo whole-cell patch-clamp recordings further demonstrated that miniature excitatory and inhibitory synaptic currents in CA1 pyramidal neurons underwent experience-specific reorganization. Together, these findings support a coordinated cascade in which episodic experience induces population-level ensemble activity, followed by diversification of ripple firing patterns and reorganization of excitatory and inhibitory synaptic inputs in hippocampal CA1. This coordination defines a population-level signature associated with experience-dependent encoding across hippocampal circuits. Key points The hippocampus is essential for episodic memory, but how real-life experiences change brain activity and synaptic connections remains unclear. In freely moving rats, emotionally salient experiences triggered brief bursts of high-frequency firing involving many neurons in the hippocampal CA1 region (“super bursts”). After these experiences, short high-frequency firing events linked to memory processing (“ripple firing”) became more diverse in their timing and shape. Recordings from individual neurons showed that both excitatory and inhibitory synaptic inputs were reorganized in an experience-specific manner. These results suggest that episodic experience is encoded through coordinated changes in population activity, ripple firing patterns, and synaptic inputs in hippocampal CA1.