Exposure to sounds during sleep impairs hippocampal sharp wave ripples and memory consolidation

Abstract

Sleep is critical for the consolidation of recent experiences into long-term memories. As a key underlying neuronal mechanism, hippocampal sharp-wave ripples (SWRs) occurring during sleep define periods of hippocampal reactivation of recent experiences and have been causally linked with memory consolidation. Hippocampal SWR-dependent memory consolidation during sleep is often referred to as occurring during an "offline" state, dedicated to processing internally generated neural activity patterns rather than external stimuli. However, the brain is not fully disconnected from the environment during sleep. In particular, sounds heard during sleep are processed by a highly active auditory system which projects to brain regions in the medial temporal lobe, reflecting an anatomical pathway for sound modulation of hippocampal activity. While neural processing of salient sounds during sleep, such as those of a predator or an offspring, is evolutionarily adaptive, whether ongoing processing of environmental sounds during sleep interferes with SWR-dependent memory consolidation remains unknown. To address this question, we used a closed-loop system to deliver non-waking sound stimuli during or following SWRs in sleeping rats. We found that exposure to sounds during sleep suppressed the ripple power and reduced the rate of SWRs. Furthermore, sounds delivered during SWRs (On-SWR) suppressed ripple power significantly more than sounds delivered 2 seconds after SWRs (Off-SWR). Next, we tested the influence of sound presentation during sleep on memory consolidation. To this end, SWR-triggered sounds were applied during sleep sessions following learning of a conditioned place preference paradigm, in which rats learned a place-reward association. We found that On-SWR sound pairing during post-learning sleep induced a complete abolishment of memory retention 24 h following learning, while leaving memory retention immediately following sleep intact. In contrast, Off-SWR pairing weakened memory 24 h following learning as well as immediately following learning. Notably, On-SWR pairing induced a significantly larger impairment in memory 24 h after learning as compared to Off-SWR pairing. Together, these findings suggest that sounds heard during sleep suppress SWRs and memory consolidation, and that the magnitude of these effects are dependent on sound-SWR timing. These results suggest that exposure to environmental sounds during sleep may pose a risk for memory consolidation processes.