Local awakening: Regional reorganizations of brain oscillations after sleep

Brain functions express rhythmic fluctuations accompanied by sleep and wakefulness each day, but how sleep regulates brain rhythms remains unclear. Following the dose-dependent local sleep concept, two succeeding questions emerge: (1) is the sleep regulation a network-specific process; and (2) is the awakening state dependent on the previous sleep stages? To answer the questions, we conducted simultaneous EEG and fMRI recordings over 22 healthy male participants, along pre-sleep, nocturnal sleep and awakening. Using paired comparisons between awakening and pre-sleep conditions, three scenarios of the regional specificity were demonstrated on awakening: (1) the default-mode and hippocampal networks maintained similar connectivity and spectral power; (2) the sensorimotor network presented reduced connectivity and spectral power; and (3) the thalamus demonstrated substantially enhanced connectivity to the neo-cortex with decreased spectral power. With regard to the stage effect, the deep sleep group had significant changes in both functional connectivity and spectral power on awakening, whereas the indices of light sleep group remained relatively quiescent after sleep. The phenomena implied that slow-wave sleep could be key to rebooting the BOLD fluctuations after sleep. In conclusion, the regional specificity and the stage effect were verified in support of the local awakening concept, indicating that sleep regulation leads to the reorganization of brain networks upon awakening.

[1]  Archana Venkataraman,et al.  Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. , 2010, Journal of neurophysiology.

[2]  Noriko Matsuura,et al.  Preparation for awakening: self-awakening vs. forced awakening preparatory hangs in the pre-awakening period. , 2010, International review of neurobiology.

[3]  Maria Concetta Pellicciari,et al.  The electroencephalographic substratum of the awakening , 2006, Behavioural Brain Research.

[4]  A. Braun,et al.  Decoupling of the brain's default mode network during deep sleep , 2009, Proceedings of the National Academy of Sciences.

[5]  A. Karni,et al.  Dependence on REM sleep of overnight improvement of a perceptual skill. , 1994, Science.

[6]  M. Walker,et al.  Sleep Deprivation Amplifies Reactivity of Brain Reward Networks, Biasing the Appraisal of Positive Emotional Experiences , 2011, The Journal of Neuroscience.

[7]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[8]  G. Tononi,et al.  Breakdown of Cortical Effective Connectivity During Sleep , 2005, Science.

[9]  T. Kuboyama,et al.  Changes in cerebral blood flow velocity in healthy young men during overnight sleep and while awake. , 1997, Electroencephalography and clinical neurophysiology.

[10]  E. Mignot.  Why We Sleep: The Temporal Organization of Recovery , 2008, PLoS biology.

[11]  Yufeng Zang,et al.  Spontaneous Brain Activity in the Default Mode Network Is Sensitive to Different Resting-State Conditions with Limited Cognitive Load , 2009, PloS one.

[12]  R. Stickgold,et al.  Sleep, memory, and plasticity. , 2006, Annual review of psychology.

[13]  M. Raichle,et al.  Cortical network functional connectivity in the descent to sleep , 2009, Proceedings of the National Academy of Sciences.

[14]  M. Boly,et al.  Breakdown of within- and between-network Resting State Functional Magnetic Resonance Imaging Connectivity during Propofol-induced Loss of Consciousness , 2010, Anesthesiology.

[15]  P. Achermann,et al.  Sleep Homeostasis and Models of Sleep Regulation , 1999 .

[16]  Matthew P Walker,et al.  Sleep Facilitates Consolidation of Emotional Declarative Memory , 2006, Psychological science.

[17]  Pierre Philip,et al.  The circadian and homeostatic modulation of sleep pressure during wakefulness differs between morning and evening chronotypes , 2003, Journal of sleep research.

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

[19]  Alain Muzet,et al.  Sleep inertia. , 2000, Sleep medicine reviews.

[20]  Guang H. Yue,et al.  Reductions in interhemispheric motor cortex functional connectivity after muscle fatigue , 2005, Brain Research.

[21]  G. Pelled,et al.  Different physiological MRI noise between cortical layers , 2004, Magnetic resonance in medicine.

[22]  Manuel Schabus,et al.  Functional neuroimaging insights into the physiology of human sleep. , 2010, Sleep.

[23]  Kwang Suk Park,et al.  Nocturnal Awakening and Sleep Efficiency Estimation Using Unobtrusively Measured Ballistocardiogram , 2014, IEEE Transactions on Biomedical Engineering.

[24]  Chaozhe Zhu,et al.  Amplitude of low frequency fluctuation within visual areas revealed by resting-state functional MRI , 2007, NeuroImage.

[25]  A R McIntosh,et al.  The development of a noisy brain. , 2010, Archives italiennes de biologie.

[26]  Ursula Voss,et al.  Changes in EEG pre and post awakening. , 2010, International review of neurobiology.

[27]  Michael M. Halassa,et al.  Thalamocortical dynamics of sleep: roles of purinergic neuromodulation. , 2011, Seminars in cell & developmental biology.

[28]  Giulio Tononi,et al.  Local experience-dependent changes in the wake EEG after prolonged wakefulness. , 2013, Sleep.

[29]  Alan C. Evans,et al.  Regional Cerebral Blood Flow Changes as a Function of Delta and Spindle Activity during Slow Wave Sleep in Humans , 1997, The Journal of Neuroscience.

[30]  Hiroki Ikeda,et al.  Effect of sleep inertia on switch cost and arousal level immediately after awakening from normal nocturnal sleep , 2008 .

[31]  Athena Demertzi,et al.  Thalamus, Brainstem and Salience Network Connectivity Changes During Propofol-Induced Sedation and Unconsciousness , 2013, Brain Connect..

[32]  Maximilian Reiser,et al.  Classifying fMRI-derived resting-state connectivity patterns according to their daily rhythmicity , 2013, NeuroImage.

[33]  H. Hwu,et al.  Frequency‐specific alternations in the amplitude of low‐frequency fluctuations in schizophrenia , 2014, Human brain mapping.

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

[35]  M. Boly,et al.  Baseline brain activity fluctuations predict somatosensory perception in humans , 2007, Proceedings of the National Academy of Sciences.

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

[37]  DM Edgar,et al.  Effect of SCN lesions on sleep in squirrel monkeys: evidence for opponent processes in sleep-wake regulation , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  Anthony G. Hudetz,et al.  Specific and nonspecific thalamocortical functional connectivity in normal and vegetative states , 2011, Consciousness and Cognition.

[39]  G. Tononi,et al.  Local sleep and learning , 2004, Nature.

[40]  Ying Han,et al.  Frequency-dependent changes in the amplitude of low-frequency fluctuations in amnestic mild cognitive impairment: A resting-state fMRI study , 2011, NeuroImage.

[41]  Till Roenneberg,et al.  Chronobiology: The human sleep project , 2013, Nature.

[42]  N. Kleitman,et al.  Regularly occurring periods of eye motility, and concomitant phenomena, during sleep. , 1953, Science.

[43]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[44]  M. Ferrara,et al.  Electroencephalographic sleep inertia of the awakening brain , 2011, Neuroscience.

[45]  Arvind P Pathak,et al.  Decoupling of the Hemodynamic and Activation-induced Delays in Functional Magnetic Resonance Imaging , 2003, Journal of computer assisted tomography.

[46]  Xi-Nian Zuo,et al.  REST: A Toolkit for Resting-State Functional Magnetic Resonance Imaging Data Processing , 2011, PloS one.

[47]  Vincenzo Crunelli,et al.  Infraslow (<0.1 Hz) oscillations in thalamic relay nuclei basic mechanisms and significance to health and disease states. , 2011, Progress in brain research.

[48]  A. Muzet,et al.  Sleep inertia. , 2000, Sleep medicine reviews.

[49]  M. Czisch,et al.  Development of the brain's default mode network from wakefulness to slow wave sleep. , 2011, Cerebral cortex.

[50]  Peter Herscovitch,et al.  The process of awakening: a PET study of regional brain activity patterns mediating the re-establishment of alertness and consciousness. , 2002, Brain : a journal of neurology.

[51]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[52]  I Oswald,et al.  Sleep Is for Tissue Restoration , 1977, Journal of the Royal College of Physicians of London.