Journal Article

Sensory Encoding Alternates With Hippocampal Ripples across Cycles of Forebrain Spiking Cascades

Duyn, Jeff H., Leopold, David A., Liu, Xiao, Yang, Yifan, Sipe, Grayson O.

2025

Overview

The brain's response to external events depends on its internal arousal states, which are dynamically governed by neuromodulatory systems and have recently been linked to coordinated spike timing cascades in widespread brain networks. At rest, both arousal fluctuations and spiking cascades are evident throughout the forebrain and play out over multisecond time scales. Here, by analyzing large‐scale neural recording data collected by the Allen Institute, it is demonstrated that these intrinsic processes persist across the mouse brain even during periods of continuous visual stimulation. In the stationary animal, each quasi‐periodic cascade cycle systematically influenced 1) the efficacy of encoding in visually responsive brain areas and 2) the incidence of memory‐related hippocampal ripples. During this cycle, the phase of high arousal is marked by high efficiency in visual encoding whereas the phase of low arousal is marked by the occurrence of hippocampal ripples. However, during bouts of active locomotion, this cycle is abolished and brain maintained a state of elevated visual coding efficiency, with ripples being nearly absent. It is hypothesized that the infra‐slow cascade dynamics reflect an adaptive cycle of alternating exteroceptive sensory sampling and internal mnemonic function that persistently pervades the forebrain, only stopping during active exploration of the environment. This study reveals widespread, coordinated brain activity during passive visual stimulation in mice. Sensory coding, phase‐locked with the periodic dynamics, shows an inverse relationship to hippocampal ripples. The results suggest that periodic brain activity spurs alteration between two distinct operational modes of brain, facilitating exteroceptive sensory sampling and internal mnemonic processes, respectively.

• Publisher: John Wiley & Sons, Inc,John Wiley and Sons Inc,Wiley
• Subject: Action Potentials - physiology / Animals / Arousal - physiology / Behavior / brain states / global signal / hippocampal ripples / Hippocampus - physiology / low‐frequency neuronal population dynamics / Male / Mice / Mice, Inbred C57BL / neural coding / Photic Stimulation / Prosencephalon - physiology