Episodic experience drives ripple reorganization and synaptic changes in the hippocampus

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 pointsO_LIThe hippocampus is essential for episodic memory, but how real-life experiences change brain activity and synaptic connections remains unclear. C_LIO_LIIn freely moving rats, emotionally salient experiences triggered brief bursts of high-frequency firing involving many neurons in the hippocampal CA1 region ("super bursts"). C_LIO_LIAfter these experiences, short high-frequency firing events linked to memory processing ("ripple firing") became more diverse in their timing and shape. C_LIO_LIRecordings from individual neurons showed that both excitatory and inhibitory synaptic inputs were reorganized in an experience-specific manner. C_LIO_LIThese results suggest that episodic experience is encoded through coordinated changes in population activity, ripple firing patterns, and synaptic inputs in hippocampal CA1. C_LI