Replay of large-scale spatio-temporal patterns from waking during subsequent NREM sleep in human cortex

Xi Jiang,Eric Halgren,Daniel Friedman,Thomas Thesen,Orrin Devinsky,Emad Eskandar,Werner K Doyle,Patricia Dugan,Sydney S Cash,Isaac Shamie

doi:10.1038/s41598-017-17469-w

Abstract

Animal studies support the hypothesis that in slow-wave sleep, replay of waking neocortical activity under hippocampal guidance leads to memory consolidation. However, no intracranial electrophysiological evidence for replay exists in humans. We identified consistent sequences of population firing peaks across widespread cortical regions during complete waking periods. The occurrence of these “Motifs” were compared between sleeps preceding the waking period (“Sleep-Pre”) when the Motifs were identified, and those following (“Sleep-Post”). In all subjects, the majority of waking Motifs (most of which were novel) had more matches in Sleep-Post than in Sleep-Pre. In rodents, hippocampal replay occurs during local sharp-wave ripples, and the associated neocortical replay tends to occur during local sleep spindles and down-to-up transitions. These waves may facilitate consolidation by sequencing cell-firing and encouraging plasticity. Similarly, we found that Motifs were coupled to neocortical spindles, down-to-up transitions, theta bursts, and hippocampal sharp-wave ripples. While Motifs occurring during cognitive task performance were more likely to have more matches in subsequent sleep, our studies provide no direct demonstration that the replay of Motifs contributes to consolidation. Nonetheless, these results confirm a core prediction of the dominant neurobiological theory of human memory consolidation.

Highlights

“Replay” of spatio-temporal neuronal activity patterns from waking during slow-wave sleep (SWS) was first demonstrated in rat hippocampal place cells[1,2]
We reasoned that distributed spatio-temporal patterns of sequential High Gamma (HG) amplitude peaks would be found if we searched in 6–19 hours of continuous waking ECoG/SEEG
Widespread cortical Motifs were identified during waking, and spatiotemporal activity patterns similar to those Motifs were identified from the two NREM periods that comprise Sleep-Post and the two NREM periods that comprise Sleep-Pre

Summary

Introduction

“Replay” of spatio-temporal neuronal activity patterns from waking during slow-wave sleep (SWS) was first demonstrated in rat hippocampal place cells[1,2]. In addition to spindles and delta activities, whose phasic coupling to ripples appears to enhance consolidation[26], there have been reports of cortical theta oscillations coordinating sequential encoding of episodic memory[27] and their occurrence in NREM sleep being predictive of successful verbal memory recall[28]. We reasoned that distributed spatio-temporal patterns of sequential HG amplitude peaks would be found if we searched in 6–19 hours of continuous waking ECoG/SEEG Based on their spatio-temporal similarity, we clustered these patterns into recurring “Motifs”. We hypothesized that these Motifs would be more prevalent during NREM periods following the waking period (“Sleep-Post”) than those preceding it (“Sleep-Pre”), indicating a “replay” of the day’s neural activities during subsequent sleeps

Methods

Results

Conclusion