Links between the brain and body during sleep: implications for memory processing

Whitehurst, Lauren N.; Subramoniam, Anjana; Krystal, Andrew D.; Prather, Aric A.

doi:10.1016/j.tins.2021.12.007

Cited by 13 publications

(15 citation statements)

References 131 publications

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“…( 16 ) provide novel insights into the overlooked influence of the autonomic nervous system (ANS) on sleep-dependent memory mechanisms. The ANS shows clear physiologic shifts across wake and sleep stages and has recently been implicated in sleep-dependent cognition ( 17 ). In their review of the literature, these authors provide robust evidence for two distinct ANS–central nervous system networks, in which electrophysiologic features and changes in heart rate beats, known as heart rate variability, are interconnected and facilitate either the consolidation of episodic memory or performance gains in working memory.…”

Section: Sleep Within the Brain And How It Is Influenced By The Bodymentioning

confidence: 99%

The functions of sleep: A cognitive neuroscience perspective

Simon

Nadel

Payne

2022

Proc. Natl. Acad. Sci. U.S.A.

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This Special Feature explores the various purposes served by sleep, describing current attempts to understand how the many functions of sleep are instantiated in neural circuits and cognitive structures. Our feature reflects current experts' opinions about, and insights into, the dynamic processes of sleep. In the last few decades, technological advances have supported the updated view that sleep plays an active role in both cognition and health. However, these roles are far from understood. This collection of articles evaluates the dynamic nature of sleep, how it evolves across the lifespan, becomes a competitive arena for memory systems through the influence of the autonomic system, supports the consolidation and integration of new memories, and how lucid dreams might originate. This set of papers highlights new approaches and insights that will lay the groundwork to eventually understand the full range of functions supported by sleep.

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Section: Sleep Within the Brain And How It Is Influenced By The Bodymentioning

confidence: 99%

The functions of sleep: A cognitive neuroscience perspective

Simon

Nadel

Payne

2022

Proc. Natl. Acad. Sci. U.S.A.

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“…The autonomic nervous system (ANS) is divided into two branches, with the sympathetic branch associated with energy mobilization during so-called fight–flight–freeze responses ( 1 , 2 ) and the parasympathetic branch associated with vegetative and restorative functions during so-called rest–digest responses ( 3 ). These branches “work antagonistically, synergistically, and independently to gather information from sensory organs and coordinate responses to internal and external demands” ( 4 ). Both the sympathetic and parasympathetic nervous systems communicate with the central nervous system (CNS), forming a system named the central autonomic network.…”

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confidence: 99%

“…For a recent review of the brain areas and neuromodulatory systems comprising the parasympathetic and sympathetic branches, as well as their inputs to brain areas devoted to cognitive processing, see Whitehurst et al. ( 4 ).…”

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confidence: 99%

Understanding the roles of central and autonomic activity during sleep in the improvement of working memory and episodic memory

Chen

Zhang

Thayer

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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The last decade has seen significant progress in identifying sleep mechanisms that support cognition. Most of these studies focus on the link between electrophysiological events of the central nervous system during sleep and improvements in different cognitive domains, while the dynamic shifts of the autonomic nervous system across sleep have been largely overlooked. Recent studies, however, have identified significant contributions of autonomic inputs during sleep to cognition. Yet, there remain considerable gaps in understanding how central and autonomic systems work together during sleep to facilitate cognitive improvement. In this article we examine the evidence for the independent and interactive roles of central and autonomic activities during sleep and wake in cognitive processing. We specifically focus on the prefrontal–subcortical structures supporting working memory and mechanisms underlying the formation of hippocampal-dependent episodic memory. Our Slow Oscillation Switch Model identifies separate and competing underlying mechanisms supporting the two memory domains at the synaptic, systems, and behavioral levels. We propose that sleep is a competitive arena in which both memory domains vie for limited resources, experimentally demonstrated when boosting one system leads to a functional trade-off in electrophysiological and behavioral outcomes. As these findings inevitably lead to further questions, we suggest areas of future research to better understand how the brain and body interact to support a wide range of cognitive domains during a single sleep episode.

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“…Consistent with this, high vagal tone is associated with better extinction learning in humans [41–43], and enhancing vagal activity improves extinction learning and retention of extinction memory in both rodents [44–48] and humans [49–51]. In addition, a separate line of recent studies shows that vagal activity during sleep, as indexed by HF-HRV, independently contributes to memory consolidation over and above contributions by sleep architecture and sleep-related brain oscillations [52,53]. However, no study to date has examined the role of vagal activity in the sleep-dependent consolidation of extinction memory in any population.…”

Section: Introductionmentioning

confidence: 99%

REM disruption and REM Vagal Activity Predict Extinction Recall in Trauma-Exposed Individuals

Yuksel,

Watford,

Muranaka

et al. 2023

Preprint

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Accumulating evidence suggests that rapid eye movement sleep (REM) supports the consolidation of extinction memory. REM is disrupted in PTSD, and REM abnormalities after traumatic events increase the risk of developing PTSD. Therefore, it was hypothesized that abnormal REM in trauma-exposed individuals may pave the way for PTSD by interfering with the processing of extinction memory. In addition, PTSD patients display reduced vagal activity. Vagal activity contributes to the strengthening of memories, including fear extinction memory, and recent studies show that the role of vagus in memory processing extends to memory consolidation during sleep. Therefore, it is plausible that reduced vagal activity during sleep in trauma-exposed individuals may be an additional mechanism that impairs extinction memory consolidation. However, to date, the contribution of sleep vagal activity to the consolidation of extinction memory or any emotional memory has not been investigated. To test these hypotheses, we examined the association of extinction memory with REM characteristics and REM vagal activity (indexed as high-frequency heart rate variability; HF-HRV) in a large sample of trauma-exposed individuals (n=113). Consistent with our hypotheses, REM sleep characteristics (increased REM density and shortened REM latency) were associated with poorer physiological and explicit extinction memory. Furthermore, higher HF-HRV during REM was associated with better explicit extinction memory. These findings support the notion that disrupted REM may contribute to PTSD by impairing the consolidation of extinction memory and indicate the potential utility of interventions that target REM sleep characteristics and REM vagal activity in fear-related disorders.

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Links between the brain and body during sleep: implications for memory processing

Cited by 13 publications

References 131 publications

The functions of sleep: A cognitive neuroscience perspective

The functions of sleep: A cognitive neuroscience perspective

Understanding the roles of central and autonomic activity during sleep in the improvement of working memory and episodic memory

REM disruption and REM Vagal Activity Predict Extinction Recall in Trauma-Exposed Individuals

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