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Coupling between slow waves and sharp-wave ripples engages distributed neural activity during sleep in humans.

ABSTRACT: Hippocampal-dependent memory consolidation during sleep is hypothesized to depend on the synchronization of distributed neuronal ensembles, organized by the hippocampal sharp-wave ripples (SWRs, 80 to 150 Hz), subcortical/cortical slow-wave activity (SWA, 0.5 to 4 Hz), and sleep spindles (SP, 7 to 15 Hz). However, the precise role of these interactions in synchronizing subcortical/cortical neuronal activity is unclear. Here, we leverage intracranial electrophysiological recordings from the human hippocampus, amygdala, and temporal and frontal cortices to examine activity modulation and cross-regional coordination during SWRs. Hippocampal SWRs are associated with widespread modulation of high-frequency activity (HFA, 70 to 200 Hz), a measure of local neuronal activation. This peri-SWR HFA modulation is predicted by the coupling between hippocampal SWRs and local subcortical/cortical SWA or SP. Finally, local cortical SWA phase offsets and SWR amplitudes predicted functional connectivity between the frontal and temporal cortex during individual SWRs. These findings suggest a selection mechanism wherein hippocampal SWR and cortical slow-wave synchronization governs the transient engagement of distributed neuronal populations supporting hippocampal-dependent memory consolidation.

SUBMITTER: Skelin I

PROVIDER: S-EPMC8166184 | biostudies-literature | 2021 May

REPOSITORIES: biostudies-literature

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Coupling between slow waves and sharp-wave ripples engages distributed neural activity during sleep in humans.

Skelin Ivan I Zhang Haoxin H Zheng Jie J Ma Shiting S Mander Bryce A BA Kim McManus Olivia O Vadera Sumeet S Knight Robert T RT McNaughton Bruce L BL Lin Jack J JJ

Proceedings of the National Academy of Sciences of the United States of America 20210501 21

Hippocampal-dependent memory consolidation during sleep is hypothesized to depend on the synchronization of distributed neuronal ensembles, organized by the hippocampal sharp-wave ripples (SWRs, 80 to 150 Hz), subcortical/cortical slow-wave activity (SWA, 0.5 to 4 Hz), and sleep spindles (SP, 7 to 15 Hz). However, the precise role of these interactions in synchronizing subcortical/cortical neuronal activity is unclear. Here, we leverage intracranial electrophysiological recordings from the human ...[more]

PMID: 34001599

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Project description: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.

Dataset Information

Coupling between slow waves and sharp-wave ripples engages distributed neural activity during sleep in humans.

Publications

Coupling between slow waves and sharp-wave ripples engages distributed neural activity during sleep in humans.

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