Local and Widespread Slow Waves in Stable NREM Sleep: Evidence for Distinct Regulation Mechanisms

Previous work showed that two types of slow waves are temporally dissociated during the transition to sleep: widespread, large and steep slow waves predominate early in the falling asleep period (type I), while smaller, more circumscribed slow waves become more prevalent later (type II). Here, we studied the possible occurrence of these two types of slow waves in stable non-REM (NREM) sleep and explored potential differences in their regulation. A heuristic approach based on slow wave synchronization efficiency was developed and applied to high-density electroencephalographic (EEG) recordings collected during consolidated NREM sleep to identify the potential type I and type II slow waves. Slow waves with characteristics compatible with those previously described for type I and type II were identified in stable NREM sleep. Importantly, these slow waves underwent opposite changes across the night, with only type II slow waves displaying a clear homeostatic regulation. In addition, we showed that the occurrence of type I slow waves was often followed by larger type II slow waves, whereas the occurrence of type II slow waves was usually followed by smaller type I waves. Finally, type II slow waves were associated with a relative increase in spindle activity, while type I slow waves triggered periods of high-frequency activity. Our results provide evidence for the existence of two distinct slow wave synchronization processes that underlie two different types of slow waves. These slow waves may have different functional roles and mark partially distinct “micro-states” of the sleeping brain.

[1]  K Campbell,et al.  The evoked K-complex: all-or-none phenomenon? , 1992, Sleep.

[2]  P. Halász The K-complex as a special reactive sleep slow wave - A theoretical update. , 2016, Sleep medicine reviews.

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

[4]  G. Tononi,et al.  Enhancement of sleep slow waves: underlying mechanisms and practical consequences , 2014, Front. Syst. Neurosci..

[5]  Y. Nir,et al.  Local Sleep Oscillations: Implications for Memory Consolidation , 2019, Front. Neurosci..

[6]  Maria Concetta Pellicciari,et al.  Effect of total sleep deprivation on the landmarks of stage 2 sleep , 2003, Clinical Neurophysiology.

[7]  Giulio Tononi,et al.  Ultrastructural evidence for synaptic scaling across the wake/sleep cycle , 2017, Science.

[8]  P. Achermann,et al.  Low-frequency (<1Hz) oscillations in the human sleep electroencephalogram , 1997, Neuroscience.

[9]  R. Chervin Epworth sleepiness scale? , 2003, Sleep medicine.

[10]  Y. Agid,et al.  Distribution of monoaminergic, cholinergic, and GABAergic markers in the human cerebral cortex , 1989, Neuroscience.

[11]  Marcello Massimini,et al.  Sleep homeostasis and cortical synchronization: III. A high-density EEG study of sleep slow waves in humans. , 2007, Sleep.

[12]  B. Wallin,et al.  Sympathetic muscle nerve activity during sleep in man. , 1991, Brain : a journal of neurology.

[13]  Marijn C. W. Kroes,et al.  Light sleep versus slow wave sleep in memory consolidation: a question of global versus local processes? , 2014, Trends in Neurosciences.

[14]  Joshua J. LaRocque,et al.  Two distinct synchronization processes in the transition to sleep: a high-density electroencephalographic study. , 2014, Sleep.

[15]  T. Sejnowski,et al.  Interplay between spontaneous and induced brain activity during human non-rapid eye movement sleep , 2011, Proceedings of the National Academy of Sciences.

[16]  Andreas Buchmann,et al.  Sleep reverts changes in human gray and white matter caused by wake-dependent training , 2016, NeuroImage.

[17]  Sean L. Hill,et al.  Sleep homeostasis and cortical synchronization: I. Modeling the effects of synaptic strength on sleep slow waves. , 2007, Sleep.

[18]  Giulio Tononi,et al.  Triggering slow waves during NREM sleep in the rat by intracortical electrical stimulation: effects of sleep/wake history and background activity. , 2009, Journal of neurophysiology.

[19]  R. Pigeau,et al.  Effects of sleep deprivation on spontaneous arousals in humans. , 2004, Sleep.

[20]  M Steriade,et al.  Intracellular analysis of relations between the slow (< 1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  Salome Kurth,et al.  How do children fall asleep? A high-density EEG study of slow waves in the transition from wake to sleep , 2018, NeuroImage.

[22]  M. Johns,et al.  A new method for measuring daytime sleepiness: the Epworth sleepiness scale. , 1991, Sleep.

[23]  R. Verleger,et al.  Dynamic coupling between slow waves and sleep spindles during slow wave sleep in humans is modulated by functional pre-sleep activation , 2017, Scientific Reports.

[24]  S. Hughes,et al.  The slow (<1 Hz) rhythm of non-REM sleep: a dialogue between three cardinal oscillators , 2010, Nature Neuroscience.

[25]  G. Tononi,et al.  Sleep and the Price of Plasticity: From Synaptic and Cellular Homeostasis to Memory Consolidation and Integration , 2014, Neuron.

[26]  I. Feinberg,et al.  Homeostatic behavior of fast fourier transform power in very low frequency non-rapid eye movement human electroencephalogram , 2006, Neuroscience.

[27]  A. Loomis,et al.  Cerebral states during sleep, as studied by human brain potentials , 1937 .

[28]  G. Pampiglione,et al.  The effects of repeated stimuli upon EEG and vasomotor activity during sleep in man. , 1958, Brain : a journal of neurology.

[29]  M. Steriade Grouping of brain rhythms in corticothalamic systems , 2006, Neuroscience.

[30]  R. Furlan,et al.  Relationship between blood pressure, sleep K-complexes, and muscle sympathetic nerve activity in humans. , 2003, American journal of physiology. Regulatory, integrative and comparative physiology.

[31]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[32]  C. Schenck The far side of sleep: Towards a deeper understanding of parasomnias and nocturnal seizures , 2014, Sleep science.

[33]  A. Silvani,et al.  Commentary: Coordinated infraslow neural and cardiac oscillations mark fragility and offline periods in mammalian sleep , 2017, Front. Physiol..

[34]  K. Ganguly,et al.  Competing Roles of Slow Oscillations and Delta Waves in Memory Consolidation versus Forgetting , 2019, Cell.

[35]  A. Ioannides,et al.  The Emergence of Spindles and K-Complexes and the Role of the Dorsal Caudal Part of the Anterior Cingulate as the Generator of K-Complexes , 2019, Front. Neurosci..

[36]  Liborio Parrino,et al.  Cyclic alternating pattern (CAP): the marker of sleep instability. , 2012, Sleep medicine reviews.

[37]  J. Born,et al.  Coordinated infraslow neural and cardiac oscillations mark fragility and offline periods in mammalian sleep , 2017, Science Advances.

[38]  M. Steriade,et al.  Natural waking and sleep states: a view from inside neocortical neurons. , 2001, Journal of neurophysiology.

[39]  Ian M Colrain,et al.  The K-complex: a 7-decade history. , 2005, Sleep.

[40]  J. Shaw,et al.  The form voltage distribution and physiological significance of the K-complex. , 1956, Electroencephalography and clinical neurophysiology.

[41]  M. Bertini,et al.  The Cyclic Alternating Pattern Decreases as a Consequence of Total Sleep Deprivation and Correlates with EEG Arousals , 2002, Neuropsychobiology.

[42]  Arnaud Delorme,et al.  EEGLAB, SIFT, NFT, BCILAB, and ERICA: New Tools for Advanced EEG Processing , 2011, Comput. Intell. Neurosci..

[43]  G. Tononi,et al.  Triggering sleep slow waves by transcranial magnetic stimulation , 2007, Proceedings of the National Academy of Sciences.

[44]  T. Maling,et al.  The k-complex vasoconstrictor response: evidence for central vasomotor downregulation in borderline hypertension. , 1989, Journal of hypertension. Supplement : official journal of the International Society of Hypertension.

[45]  B. A. Conway,et al.  The effects of laforin, malin, Stbd1, and Ptg deficiencies on heart glycogen levels in Pompe disease mouse models , 2015 .

[46]  M. Steriade,et al.  A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  M. Ferrara,et al.  The effects of sleep deprivation in humans: topographical electroencephalogram changes in non‐rapid eye movement (NREM) sleep versus REM sleep , 2009, Journal of sleep research.

[48]  Giulio Tononi,et al.  Optimizing detection and analysis of slow waves in sleep EEG , 2016, Journal of Neuroscience Methods.

[49]  J. Born,et al.  Grouping of Spindle Activity during Slow Oscillations in Human Non-Rapid Eye Movement Sleep , 2002, The Journal of Neuroscience.

[50]  A Kok,et al.  Event‐related potentials to tones in the absence and presence of sleep spindles , 1997, Journal of sleep research.

[51]  Chris Gonzalez,et al.  Coordination of cortical and thalamic activity during non-REM sleep in humans , 2017, Nature Communications.

[52]  J. R. Smith,et al.  Automatic detection of the K-complex in sleep electroencephalograms. , 1970, IEEE transactions on bio-medical engineering.

[53]  P. Achermann,et al.  Slow oscillations in human non‐rapid eye movement sleep electroencephalogram: effects of increased sleep pressure , 2010, Journal of sleep research.

[54]  H. Laufs,et al.  The avalanche-like behaviour of large-scale haemodynamic activity from wakefulness to deep sleep , 2019, Journal of the Royal Society Interface.

[55]  Nima Dehghani,et al.  The Human K-Complex Represents an Isolated Cortical Down-State , 2009, Science.

[56]  Sean L. Hill,et al.  The Sleep Slow Oscillation as a Traveling Wave , 2004, The Journal of Neuroscience.

[57]  G. Tononi,et al.  Sleep homeostasis and cortical synchronization: II. A local field potential study of sleep slow waves in the rat. , 2007, Sleep.

[58]  Oscar Herreras,et al.  Slow-Wave Activity in the S1HL Cortex Is Contributed by Different Layer-Specific Field Potential Sources during Development , 2019, The Journal of Neuroscience.

[59]  P. Halász Arousals without awakening—Dynamic aspect of sleep , 1993, Physiology & Behavior.

[60]  K. Campbell,et al.  Effects of rate of tone‐pip stimulation on the evoked K‐Complex , 1994, Journal of sleep research.

[61]  A. Gemignani,et al.  Functional Structure of Spontaneous Sleep Slow Oscillation Activity in Humans , 2009, PloS one.

[62]  Michele Ferrara,et al.  The spontaneous K-complex during stage 2 sleep: is it the ‘forerunner’ of delta waves? , 2000, Neuroscience Letters.

[63]  J. Morrison,et al.  Noradrenergic innervation of monkey prefrontal cortex: A dopamine‐β‐hydroxylase immunohistochemical study , 1989, The Journal of comparative neurology.

[64]  B. Berger,et al.  Catecholamine innervation of the human cerebral cortex as revealed by comparative immunohistochemistry of tyrosine hydroxylase and dopamine‐beta‐hydroxylase , 1989, The Journal of comparative neurology.

[65]  P. Davis,et al.  ELECTRICAL REACTIONS OF THE HUMAN BRAIN TO AUDITORY STIMULATION DURING SLEEP , 1939 .

[66]  Dominique Hasboun,et al.  Human Gamma Oscillations during Slow Wave Sleep , 2012, PloS one.

[67]  Giulio Tononi,et al.  Temporal dynamics of cortical sources underlying spontaneous and peripherally evoked slow waves. , 2011, Progress in brain research.

[68]  M. Terzano,et al.  CAP and arousals are involved in the homeostatic and ultradian sleep processes , 2005, Journal of sleep research.

[69]  K. Harris,et al.  Sleep and the single neuron: the role of global slow oscillations in individual cell rest , 2013, Nature Reviews Neuroscience.

[70]  G. Tononi,et al.  Sleep function and synaptic homeostasis. , 2006, Sleep medicine reviews.

[71]  L. Johnson,et al.  Autonomic correlates of the spontaneous K-complex. , 1968, Psychophysiology.

[72]  Péter Halász,et al.  K-complex, a reactive EEG graphoelement of NREM sleep: an old chap in a new garment. , 2005, Sleep medicine reviews.