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Tracking the Sleep Onset Process: An Empirical Model of Behavioral and Physiological Dynamics

The sleep onset process (SOP) is a dynamic process correlated with a multitude of behavioral and physiological markers. A principled analysis of the SOP can serve as a foundation for answering questions of fundamental importance in basic neuroscience and sleep medicine. Unfortunately, current method...

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Autores principales: Prerau, Michael J., Hartnack, Katie E., Obregon-Henao, Gabriel, Sampson, Aaron, Merlino, Margaret, Gannon, Karen, Bianchi, Matt T., Ellenbogen, Jeffrey M., Purdon, Patrick L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4183428/
https://www.ncbi.nlm.nih.gov/pubmed/25275376
http://dx.doi.org/10.1371/journal.pcbi.1003866
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author Prerau, Michael J.
Hartnack, Katie E.
Obregon-Henao, Gabriel
Sampson, Aaron
Merlino, Margaret
Gannon, Karen
Bianchi, Matt T.
Ellenbogen, Jeffrey M.
Purdon, Patrick L.
author_facet Prerau, Michael J.
Hartnack, Katie E.
Obregon-Henao, Gabriel
Sampson, Aaron
Merlino, Margaret
Gannon, Karen
Bianchi, Matt T.
Ellenbogen, Jeffrey M.
Purdon, Patrick L.
author_sort Prerau, Michael J.
collection PubMed
description The sleep onset process (SOP) is a dynamic process correlated with a multitude of behavioral and physiological markers. A principled analysis of the SOP can serve as a foundation for answering questions of fundamental importance in basic neuroscience and sleep medicine. Unfortunately, current methods for analyzing the SOP fail to account for the overwhelming evidence that the wake/sleep transition is governed by continuous, dynamic physiological processes. Instead, current practices coarsely discretize sleep both in terms of state, where it is viewed as a binary (wake or sleep) process, and in time, where it is viewed as a single time point derived from subjectively scored stages in 30-second epochs, effectively eliminating SOP dynamics from the analysis. These methods also fail to integrate information from both behavioral and physiological data. It is thus imperative to resolve the mismatch between the physiological evidence and analysis methodologies. In this paper, we develop a statistically and physiologically principled dynamic framework and empirical SOP model, combining simultaneously-recorded physiological measurements with behavioral data from a novel breathing task requiring no arousing external sensory stimuli. We fit the model using data from healthy subjects, and estimate the instantaneous probability that a subject is awake during the SOP. The model successfully tracked physiological and behavioral dynamics for individual nights, and significantly outperformed the instantaneous transition models implicit in clinical definitions of sleep onset. Our framework also provides a principled means for cross-subject data alignment as a function of wake probability, allowing us to characterize and compare SOP dynamics across different populations. This analysis enabled us to quantitatively compare the EEG of subjects showing reduced alpha power with the remaining subjects at identical response probabilities. Thus, by incorporating both physiological and behavioral dynamics into our model framework, the dynamics of our analyses can finally match those observed during the SOP.
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spelling pubmed-41834282014-10-07 Tracking the Sleep Onset Process: An Empirical Model of Behavioral and Physiological Dynamics Prerau, Michael J. Hartnack, Katie E. Obregon-Henao, Gabriel Sampson, Aaron Merlino, Margaret Gannon, Karen Bianchi, Matt T. Ellenbogen, Jeffrey M. Purdon, Patrick L. PLoS Comput Biol Research Article The sleep onset process (SOP) is a dynamic process correlated with a multitude of behavioral and physiological markers. A principled analysis of the SOP can serve as a foundation for answering questions of fundamental importance in basic neuroscience and sleep medicine. Unfortunately, current methods for analyzing the SOP fail to account for the overwhelming evidence that the wake/sleep transition is governed by continuous, dynamic physiological processes. Instead, current practices coarsely discretize sleep both in terms of state, where it is viewed as a binary (wake or sleep) process, and in time, where it is viewed as a single time point derived from subjectively scored stages in 30-second epochs, effectively eliminating SOP dynamics from the analysis. These methods also fail to integrate information from both behavioral and physiological data. It is thus imperative to resolve the mismatch between the physiological evidence and analysis methodologies. In this paper, we develop a statistically and physiologically principled dynamic framework and empirical SOP model, combining simultaneously-recorded physiological measurements with behavioral data from a novel breathing task requiring no arousing external sensory stimuli. We fit the model using data from healthy subjects, and estimate the instantaneous probability that a subject is awake during the SOP. The model successfully tracked physiological and behavioral dynamics for individual nights, and significantly outperformed the instantaneous transition models implicit in clinical definitions of sleep onset. Our framework also provides a principled means for cross-subject data alignment as a function of wake probability, allowing us to characterize and compare SOP dynamics across different populations. This analysis enabled us to quantitatively compare the EEG of subjects showing reduced alpha power with the remaining subjects at identical response probabilities. Thus, by incorporating both physiological and behavioral dynamics into our model framework, the dynamics of our analyses can finally match those observed during the SOP. Public Library of Science 2014-10-02 /pmc/articles/PMC4183428/ /pubmed/25275376 http://dx.doi.org/10.1371/journal.pcbi.1003866 Text en © 2014 Prerau et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Prerau, Michael J.
Hartnack, Katie E.
Obregon-Henao, Gabriel
Sampson, Aaron
Merlino, Margaret
Gannon, Karen
Bianchi, Matt T.
Ellenbogen, Jeffrey M.
Purdon, Patrick L.
Tracking the Sleep Onset Process: An Empirical Model of Behavioral and Physiological Dynamics
title Tracking the Sleep Onset Process: An Empirical Model of Behavioral and Physiological Dynamics
title_full Tracking the Sleep Onset Process: An Empirical Model of Behavioral and Physiological Dynamics
title_fullStr Tracking the Sleep Onset Process: An Empirical Model of Behavioral and Physiological Dynamics
title_full_unstemmed Tracking the Sleep Onset Process: An Empirical Model of Behavioral and Physiological Dynamics
title_short Tracking the Sleep Onset Process: An Empirical Model of Behavioral and Physiological Dynamics
title_sort tracking the sleep onset process: an empirical model of behavioral and physiological dynamics
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4183428/
https://www.ncbi.nlm.nih.gov/pubmed/25275376
http://dx.doi.org/10.1371/journal.pcbi.1003866
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