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 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.

[1]  A. Rechtschaffen,et al.  A manual of standardized terminology, technique and scoring system for sleep stages of human subjects , 1968 .

[2]  T. Dang-Vu,et al.  Spontaneous brain rhythms predict sleep stability in the face of noise , 2010, Current Biology.

[3]  A. Rechtschaffen A manual of Standardized Terminology , 1968 .

[4]  F. Mauguière,et al.  Thalamic deactivation at sleep onset precedes that of the cerebral cortex in humans , 2010, Proceedings of the National Academy of Sciences.

[5]  Emery N Brown,et al.  Dynamic Analysis of Learning in Behavioral Experiments , 2004, The Journal of Neuroscience.

[6]  R T Wilkinson,et al.  Behavioral versus EEG-based monitoring of all-night sleep/wake patterns. , 1988, Sleep.

[7]  R. Edelberg,et al.  Cardiac rhythm effects of .125-Hz paced breathing through a resistive load: Implications for paced breathing therapy and the polyvagal theory , 1996, Biofeedback and self-regulation.

[8]  Wei Wang,et al.  Sleep disruption due to hospital noises: a prospective evaluation. , 2012, Annals of internal medicine.

[9]  Duanping Liao,et al.  Insomnia with objective short sleep duration: the most biologically severe phenotype of the disorder. , 2013, Sleep medicine reviews.

[10]  R D Ogilvie,et al.  EEG spectral analysis of the sleep-onset period in narcoleptics and normal sleepers. , 1999, Sleep.

[11]  Tadao Hori,et al.  Topographical EEG changes and the hypnagogic experience. , 1994 .

[12]  L. Tarassenko,et al.  A new approach to the analysis of the human sleep/wakefulness continuum , 1996, Journal of sleep research.

[13]  B. Efron,et al.  A Leisurely Look at the Bootstrap, the Jackknife, and , 1983 .

[14]  Pietro Badia,et al.  Behavioral control of abnormal breathing in sleep , 2004, Journal of Behavioral Medicine.

[15]  E. Wolpert A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects. , 1969 .

[16]  S. Sarasso,et al.  Local aspects of sleep: observations from intracerebral recordings in humans. , 2012, Progress in brain research.

[17]  W. Dement,et al.  Quantification of sleepiness: a new approach. , 1973, Psychophysiology.

[18]  M. Bertini,et al.  The boundary between wakefulness and sleep: quantitative electroencephalographic changes during the sleep onset period , 2001, Neuroscience.

[19]  L De Gennaro,et al.  A finger-tapping task and a reaction time task as behavioral measures of the transition from wakefulness to sleep: which task interferes less with the sleep onset process. , 1997, Sleep.

[20]  P. Davis,et al.  CHANGES IN HUMAN BRAIN POTENTIALS DURING THE ONSET OF SLEEP. , 1937, Science.

[21]  Manuel Schabus,et al.  Event‐related activity and phase locking during a psychomotor vigilance task over the course of sleep deprivation , 2011, Journal of sleep research.

[22]  P. Hauri,et al.  Wrist actigraphy in insomnia. , 1992, Sleep.

[23]  A. Rechtschaffen,et al.  Auditory Awakening Thresholds in Rem and Nrem Sleep Stages , 1966, Perceptual and motor skills.

[24]  Uri T. Eden,et al.  A General Likelihood Framework for Characterizing the Time Course of Neural Activity , 2011, Neural Computation.

[25]  Tapas Pramanik,et al.  Immediate effect of slow pace bhastrika pranayama on blood pressure and heart rate. , 2009, Journal of alternative and complementary medicine.

[26]  Stephen Perrig,et al.  Spectral analysis of the sleep onset period in primary insomnia , 2014, Clinical Neurophysiology.

[27]  G. Tononi,et al.  Local sleep in awake rats , 2011, Nature.

[28]  Emery N. Brown,et al.  A mixed filter algorithm for cognitive state estimation from simultaneously recorded continuous and binary measures of performance , 2008, Biological Cybernetics.

[29]  S. Hughes,et al.  Thalamic Mechanisms of EEG Alpha Rhythms and Their Pathological Implications , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[30]  T Hori,et al.  Topographical characteristics and principal component structure of the hypnagogic EEG. , 1997, Sleep.

[31]  Chang‐Jin Kim,et al.  State-Space Models with Regime-Switching: Classical and Gibbs Sampling Approaches with Applications , 1999 .

[32]  Michael E. Clark,et al.  Effects of paced respiration on anxiety reduction in a clinical population , 1990, Biofeedback and self-regulation.

[33]  J. Solet,et al.  Measuring sleep: accuracy, sensitivity, and specificity of wrist actigraphy compared to polysomnography. , 2013, Sleep.

[34]  G. Kitagawa,et al.  Smoothness Priors in Time Series. , 1987 .

[35]  M. Ferrara,et al.  Antero-posterior EEG changes during the wakefulness–sleep transition , 2001, Clinical Neurophysiology.

[36]  Uri T Eden,et al.  Characterizing learning by simultaneous analysis of continuous and binary measures of performance. , 2009, Journal of neurophysiology.

[37]  P Badia,et al.  Behavioral control of respiration in sleep. , 1984, Psychophysiology.

[38]  D. Léger,et al.  Societal costs of insomnia. , 2010, Sleep medicine reviews.

[39]  M. Kenward,et al.  An Introduction to the Bootstrap , 2007 .

[40]  Emery N Brown,et al.  Analysis and design of behavioral experiments to characterize population learning. , 2005, Journal of neurophysiology.

[41]  J. Santamaria,et al.  The EEG of Drowsiness in Normal Adults , 1987, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[42]  Nicola Robinson,et al.  Meditative Movement for Respiratory Function: A Systematic Review , 2014, Respiratory Care.

[43]  David Barber,et al.  Bayesian Time Series Models , 2011 .

[44]  S. Telles,et al.  Oxygen consumption during pranayamic type of very slow-rate breathing. , 1991, The Indian journal of medical research.

[45]  R T Wilkinson,et al.  The detection of sleep onset: behavioral, physiological, and subjective convergence. , 1989, Sleep.

[46]  R. Ogilvie The process of falling asleep. , 2001, Sleep medicine reviews.

[47]  S. Chokroverty,et al.  The visual scoring of sleep in adults. , 2007, Journal of clinical sleep medicine : JCSM : official publication of the American Academy of Sleep Medicine.

[48]  R. Ogilvie,et al.  The detection of sleep onset: behavioral and physiological convergence. , 1984, Psychophysiology.

[49]  Thomas J Balkin,et al.  Behavioral biomarkers of sleepiness. , 2011, Journal of clinical sleep medicine : JCSM : official publication of the American Academy of Sleep Medicine.

[50]  R D Ogilvie,et al.  Electrophysiological changes during the sleep onset period of psychophysiological insomniacs, psychiatric insomniacs, and normal sleepers. , 1995, Sleep.

[51]  P. Achermann,et al.  Fronto‐occipital EEG power gradients in human sleep , 1997, Journal of sleep research.

[52]  T Hori,et al.  Statistical features of hypnagogic EEG measured by a new scoring system. , 1996, Sleep.

[53]  A. Chesson,et al.  The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology, and Techinical Specifications , 2007 .

[54]  R. Strecker,et al.  Recent Developments in Home Sleep-Monitoring Devices , 2012, ISRN neurology.

[55]  Peter Achermann,et al.  Functional EEG topography in sleep and waking: State-dependent and state-independent features , 2006, NeuroImage.

[56]  Lino Nobili,et al.  How we fall asleep: regional and temporal differences in electroencephalographic synchronization at sleep onset. , 2013, Sleep medicine.

[57]  C Dostálek,et al.  Electroencephalographic correlates of paced breathing. , 1993, Neuroreport.

[58]  Ralph W. Gerard,et al.  Factors influencing brain potentials during sleep. , 1939 .

[59]  A. Chesson,et al.  The American Academy of Sleep Medicine (AASM) Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications , 2007 .

[60]  Melvin J. Hinich,et al.  Time Series Analysis by State Space Methods , 2001 .

[61]  I. Fried,et al.  Regional Slow Waves and Spindles in Human Sleep , 2011, Neuron.

[62]  C. Shapiro,et al.  STOP, THAT and One Hundred Other Sleep Scales , 2012 .

[63]  M. Carskadon,et al.  Excessive daytime sleepiness in man: multiple sleep latency measurement in narcoleptic and control subjects. , 1978, Electroencephalography and clinical neurophysiology.