Strengthening sleep-autonomic interaction via acoustic enhancement of slow oscillations

Daniela Grimaldi, Nelly A. Papalambros, Kathryn Jean Reid, Sabra Margaret Abbott, Roneil Gopal Malkani, Maged Gendy, Marta Iwanaszko, Rosemary I Braun, Daniel J. Sanchez, Ken Paller, Phyllis C Zee

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

Slow-wave sleep (SWS) is important for overall health since it affects many physiological processes including cardio-metabolic function. Sleep and autonomic nervous system (ANS) activity are closely coupled at anatomical and physiological levels. Sleep-related changes in autonomic function are likely the main pathway through which SWS affects many systems within the body. There are characteristic changes in ANS activity across sleep stages. Notably, in non-rapid eye-movement sleep, the progression into SWS is characterized by increased parasympathetic activity, an important measure of cardiovascular health. Experimental manipulations that enhance slow-wave activity (SWA, 0.5-4 Hz) can improve sleep-mediated memory and immune function. However, effects of SWA enhancement on autonomic regulation have not been investigated. Here, we employed an adaptive algorithm to deliver 50 ms sounds phase-locked to slow-waves, with regular pauses in stimulation (~5 s ON/~5 s OFF), in healthy young adults. We sought to determine whether acoustic enhancement of SWA altered parasympathetic activity during SWS assessed with heart rate variability (HRV), and evening-to-morning changes in HRV, plasma cortisol, and blood pressure. Stimulation, compared with a sham condition, increased SWA during ON versus OFF intervals. This ON/OFF SWA enhancement was associated with a reduction in evening-to-morning change of cortisol levels and indices of sympathetic activity. Furthermore, the enhancement of SWA in ON intervals during sleep cycles 2-3 was accompanied by an increase in parasympathetic activity (high-frequency, HRV). Together these findings suggest that acoustic enhancement of SWA has a positive effect on autonomic function in sleep. Approaches to strengthen brain-heart interaction during sleep could have important implications for cardiovascular health.

Original languageEnglish (US)
Article numberzsz036
JournalSleep
Volume42
Issue number5
DOIs
StatePublished - May 1 2019

Fingerprint

Acoustics
Sleep
Heart Rate
Autonomic Nervous System
Hydrocortisone
Health
Physiological Phenomena
Sleep Stages
Eye Movements
Young Adult
Blood Pressure
Brain

Keywords

  • Acoustic stimulation
  • Autonomic nervous system
  • Parasympathetic activity
  • Sleep
  • Slow wave activity

ASJC Scopus subject areas

  • Clinical Neurology
  • Physiology (medical)

Cite this

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title = "Strengthening sleep-autonomic interaction via acoustic enhancement of slow oscillations",
abstract = "Slow-wave sleep (SWS) is important for overall health since it affects many physiological processes including cardio-metabolic function. Sleep and autonomic nervous system (ANS) activity are closely coupled at anatomical and physiological levels. Sleep-related changes in autonomic function are likely the main pathway through which SWS affects many systems within the body. There are characteristic changes in ANS activity across sleep stages. Notably, in non-rapid eye-movement sleep, the progression into SWS is characterized by increased parasympathetic activity, an important measure of cardiovascular health. Experimental manipulations that enhance slow-wave activity (SWA, 0.5-4 Hz) can improve sleep-mediated memory and immune function. However, effects of SWA enhancement on autonomic regulation have not been investigated. Here, we employed an adaptive algorithm to deliver 50 ms sounds phase-locked to slow-waves, with regular pauses in stimulation (~5 s ON/~5 s OFF), in healthy young adults. We sought to determine whether acoustic enhancement of SWA altered parasympathetic activity during SWS assessed with heart rate variability (HRV), and evening-to-morning changes in HRV, plasma cortisol, and blood pressure. Stimulation, compared with a sham condition, increased SWA during ON versus OFF intervals. This ON/OFF SWA enhancement was associated with a reduction in evening-to-morning change of cortisol levels and indices of sympathetic activity. Furthermore, the enhancement of SWA in ON intervals during sleep cycles 2-3 was accompanied by an increase in parasympathetic activity (high-frequency, HRV). Together these findings suggest that acoustic enhancement of SWA has a positive effect on autonomic function in sleep. Approaches to strengthen brain-heart interaction during sleep could have important implications for cardiovascular health.",
keywords = "Acoustic stimulation, Autonomic nervous system, Parasympathetic activity, Sleep, Slow wave activity",
author = "Daniela Grimaldi and Papalambros, {Nelly A.} and Reid, {Kathryn Jean} and Abbott, {Sabra Margaret} and Malkani, {Roneil Gopal} and Maged Gendy and Marta Iwanaszko and Braun, {Rosemary I} and Sanchez, {Daniel J.} and Ken Paller and Zee, {Phyllis C}",
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Strengthening sleep-autonomic interaction via acoustic enhancement of slow oscillations. / Grimaldi, Daniela; Papalambros, Nelly A.; Reid, Kathryn Jean; Abbott, Sabra Margaret; Malkani, Roneil Gopal; Gendy, Maged; Iwanaszko, Marta; Braun, Rosemary I; Sanchez, Daniel J.; Paller, Ken; Zee, Phyllis C.

In: Sleep, Vol. 42, No. 5, zsz036, 01.05.2019.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Strengthening sleep-autonomic interaction via acoustic enhancement of slow oscillations

AU - Grimaldi, Daniela

AU - Papalambros, Nelly A.

AU - Reid, Kathryn Jean

AU - Abbott, Sabra Margaret

AU - Malkani, Roneil Gopal

AU - Gendy, Maged

AU - Iwanaszko, Marta

AU - Braun, Rosemary I

AU - Sanchez, Daniel J.

AU - Paller, Ken

AU - Zee, Phyllis C

PY - 2019/5/1

Y1 - 2019/5/1

N2 - Slow-wave sleep (SWS) is important for overall health since it affects many physiological processes including cardio-metabolic function. Sleep and autonomic nervous system (ANS) activity are closely coupled at anatomical and physiological levels. Sleep-related changes in autonomic function are likely the main pathway through which SWS affects many systems within the body. There are characteristic changes in ANS activity across sleep stages. Notably, in non-rapid eye-movement sleep, the progression into SWS is characterized by increased parasympathetic activity, an important measure of cardiovascular health. Experimental manipulations that enhance slow-wave activity (SWA, 0.5-4 Hz) can improve sleep-mediated memory and immune function. However, effects of SWA enhancement on autonomic regulation have not been investigated. Here, we employed an adaptive algorithm to deliver 50 ms sounds phase-locked to slow-waves, with regular pauses in stimulation (~5 s ON/~5 s OFF), in healthy young adults. We sought to determine whether acoustic enhancement of SWA altered parasympathetic activity during SWS assessed with heart rate variability (HRV), and evening-to-morning changes in HRV, plasma cortisol, and blood pressure. Stimulation, compared with a sham condition, increased SWA during ON versus OFF intervals. This ON/OFF SWA enhancement was associated with a reduction in evening-to-morning change of cortisol levels and indices of sympathetic activity. Furthermore, the enhancement of SWA in ON intervals during sleep cycles 2-3 was accompanied by an increase in parasympathetic activity (high-frequency, HRV). Together these findings suggest that acoustic enhancement of SWA has a positive effect on autonomic function in sleep. Approaches to strengthen brain-heart interaction during sleep could have important implications for cardiovascular health.

AB - Slow-wave sleep (SWS) is important for overall health since it affects many physiological processes including cardio-metabolic function. Sleep and autonomic nervous system (ANS) activity are closely coupled at anatomical and physiological levels. Sleep-related changes in autonomic function are likely the main pathway through which SWS affects many systems within the body. There are characteristic changes in ANS activity across sleep stages. Notably, in non-rapid eye-movement sleep, the progression into SWS is characterized by increased parasympathetic activity, an important measure of cardiovascular health. Experimental manipulations that enhance slow-wave activity (SWA, 0.5-4 Hz) can improve sleep-mediated memory and immune function. However, effects of SWA enhancement on autonomic regulation have not been investigated. Here, we employed an adaptive algorithm to deliver 50 ms sounds phase-locked to slow-waves, with regular pauses in stimulation (~5 s ON/~5 s OFF), in healthy young adults. We sought to determine whether acoustic enhancement of SWA altered parasympathetic activity during SWS assessed with heart rate variability (HRV), and evening-to-morning changes in HRV, plasma cortisol, and blood pressure. Stimulation, compared with a sham condition, increased SWA during ON versus OFF intervals. This ON/OFF SWA enhancement was associated with a reduction in evening-to-morning change of cortisol levels and indices of sympathetic activity. Furthermore, the enhancement of SWA in ON intervals during sleep cycles 2-3 was accompanied by an increase in parasympathetic activity (high-frequency, HRV). Together these findings suggest that acoustic enhancement of SWA has a positive effect on autonomic function in sleep. Approaches to strengthen brain-heart interaction during sleep could have important implications for cardiovascular health.

KW - Acoustic stimulation

KW - Autonomic nervous system

KW - Parasympathetic activity

KW - Sleep

KW - Slow wave activity

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