Cortical network functional connectivity in the descent to sleep

Descent into sleep is accompanied by disengagement of the conscious brain from the external world. It follows that this process should be associated with reduced neural activity in regions of the brain known to mediate interaction with the environment. We examined blood oxygen dependent (BOLD) signal functional connectivity using conventional seed-based analyses in 3 primary sensory and 3 association networks as normal young adults transitioned from wakefulness to light sleep while lying immobile in the bore of a magnetic resonance imaging scanner. Functional connectivity was maintained in each network throughout all examined states of arousal. Indeed, correlations within the dorsal attention network modestly but significantly increased during light sleep compared to wakefulness. Moreover, our data suggest that neuronally mediated BOLD signal variance generally increases in light sleep. These results do not support the view that ongoing BOLD fluctuations primarily reflect unconstrained cognition. Rather, accumulating evidence supports the hypothesis that spontaneous BOLD fluctuations reflect processes that maintain the integrity of functional systems in the brain.

[1]  P. Welch The use of fast Fourier transform for the estimation of power spectra: A method based on time averaging over short, modified periodograms , 1967 .

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

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

[4]  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.

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

[6]  M Steriade,et al.  Low-frequency rhythms in the thalamus of intact-cortex and decorticated cats. , 1996, Journal of neurophysiology.

[7]  A. Braun,et al.  Regional cerebral blood flow throughout the sleep-wake cycle. An H2(15)O PET study. , 1997, Brain : a journal of neurology.

[8]  L. Lemieux,et al.  Recording of EEG during fMRI experiments: Patient safety , 1997, Magnetic resonance in medicine.

[9]  A. Braun,et al.  Regional cerebral blood flow throughout the sleep- wake cycle , 1997 .

[10]  M. Raichle,et al.  Anatomic Localization and Quantitative Analysis of Gradient Refocused Echo-Planar fMRI Susceptibility Artifacts , 1997, NeuroImage.

[11]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: II. Decreases in Cerebral Cortex , 1997, Journal of Cognitive Neuroscience.

[12]  Louis Lemieux,et al.  Identification of EEG Events in the MR Scanner: The Problem of Pulse Artifact and a Method for Its Subtraction , 1998, NeuroImage.

[13]  J. Armony,et al.  Auditory Processing across the Sleep-Wake Cycle Simultaneous EEG and fMRI Monitoring in Humans , 2000, Neuron.

[14]  T. Sejnowski,et al.  Origin of slow cortical oscillations in deafferented cortical slabs. , 2000, Cerebral cortex.

[15]  Maquet,et al.  Functional neuroimaging of normal human sleep by positron emission tomography , 2000, Journal of sleep research.

[16]  R. Amici,et al.  Changes in REM sleep occurrence due to rhythmical auditory stimulation in the rat , 2000, Brain Research.

[17]  N. Cozzarelli PNAS Early Edition. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[18]  M. Johns,et al.  Sensitivity and specificity of the multiple sleep latency test (MSLT), the maintenance of wakefulness test and the Epworth sleepiness scale: Failure of the MSLT as a gold standard , 2000, Journal of sleep research.

[19]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[20]  David C. Van Essen,et al.  Application of Information Technology: An Integrated Software Suite for Surface-based Analyses of Cerebral Cortex , 2001, J. Am. Medical Informatics Assoc..

[21]  G. Shulman,et al.  Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[22]  R. Amici,et al.  REM sleep enhancement due to rhythmical auditory stimulation in the rat , 2001, Behavioural Brain Research.

[23]  P. Maquet,et al.  Sleep imaging and the neuro-psychological assessment of dreams , 2002, Trends in Cognitive Sciences.

[24]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[25]  Daniel J Buysse,et al.  Human regional cerebral glucose metabolism during non-rapid eye movement sleep in relation to waking. , 2002, Brain : a journal of neurology.

[26]  T. Kjaer,et al.  Regional cerebral blood flow during light sleep – a H215O‐PET study , 2002, Journal of sleep research.

[27]  J. Hobson,et al.  The cognitive neuroscience of sleep: neuronal systems, consciousness and learning , 2002, Nature Reviews Neuroscience.

[28]  Misha Tsodyks,et al.  Context-enabled learning in the human visual system , 2002, Nature.

[29]  Christian Kaufmann,et al.  Altered Processing of Acoustic Stimuli during Sleep: Reduced Auditory Activation and Visual Deactivation Detected by a Combined fMRI/EEG Study , 2002, NeuroImage.

[30]  Ian M Colrain,et al.  Event-related potential measures of the inhibition of information processing: II. The sleep onset period. , 2002, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[31]  S. Aalto,et al.  Effects of Surgical Levels of Propofol and Sevoflurane Anesthesia on Cerebral Blood Flow in Healthy Subjects Studied with Positron Emission Tomography , 2002, Anesthesiology.

[32]  Hisashi Tanaka,et al.  Effect of stage 1 sleep on auditory cortex during pure tone stimulation: evaluation by functional magnetic resonance imaging with simultaneous EEG monitoring. , 2003, AJNR. American journal of neuroradiology.

[33]  S. Stansfeld,et al.  Noise pollution: non-auditory effects on health. , 2003, British medical bulletin.

[34]  M. Ferrara,et al.  Sleep spindles: an overview. , 2003, Sleep medicine reviews.

[35]  E. Darcy Burgund,et al.  Comparison of functional activation foci in children and adults using a common stereotactic space , 2003, NeuroImage.

[36]  G. Tononi,et al.  Sleep and synaptic homeostasis: a hypothesis , 2003, Brain Research Bulletin.

[37]  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.

[38]  S. Nelson,et al.  Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation , 2004, Nature Neuroscience.

[39]  Wei Lu,et al.  Eye Opening Rapidly Induces Synaptic Potentiation and Refinement , 2004, Neuron.

[40]  Christian Kaufmann,et al.  Functional MRI during sleep: BOLD signal decreases and their electrophysiological correlates , 2004, The European journal of neuroscience.

[41]  Stephen M. Smith,et al.  Investigations into resting-state connectivity using independent component analysis , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[42]  Rami K. Niazy,et al.  Removal of FMRI environment artifacts from EEG data using optimal basis sets , 2005, NeuroImage.

[43]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[44]  O. Tervonen,et al.  Midazolam sedation increases fluctuation and synchrony of the resting brain BOLD signal. , 2005, Magnetic resonance imaging.

[45]  Christophe Phillips,et al.  Cerebral correlates of delta waves during non-REM sleep revisited , 2005, NeuroImage.

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

[47]  F. Shellock,et al.  Effects of coil dimensions and field polarization on RF heating inside a head phantom. , 2005, Magnetic resonance imaging.

[48]  Steven Laureys The neural correlate of (un)awareness: lessons from the vegetative state , 2005, Trends in Cognitive Sciences.

[49]  D. V. van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex. , 2005, NeuroImage.

[50]  David C. Van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex , 2005, NeuroImage.

[51]  M. Boly,et al.  Human cognition during REM sleep and the activity profile within frontal and parietal cortices: a reappraisal of functional neuroimaging data. , 2005, Progress in brain research.

[52]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[53]  H. Schulz,et al.  A taxonomic analysis of sleep stages. , 2006, Sleep.

[54]  Peter A. Bandettini,et al.  Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI , 2006, NeuroImage.

[55]  S. Ichinose,et al.  Extension of Corticocortical Afferents into the Anterior Bank of the Intraparietal Sulcus by Tool-use Training in Adult Monkeys , 2005 .

[56]  Benjamin J. Shannon,et al.  Coherent spontaneous activity identifies a hippocampal-parietal memory network. , 2006, Journal of neurophysiology.

[57]  Roel H. R. Deckers,et al.  Large-amplitude, spatially correlated fluctuations in BOLD fMRI signals during extended rest and early sleep stages. , 2006, Magnetic resonance imaging.

[58]  Kristina M. Visscher,et al.  A Core System for the Implementation of Task Sets , 2006, Neuron.

[59]  Justin L. Vincent,et al.  Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

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

[61]  Jeong‐Wook Ghim,et al.  Learning-Induced Enduring Changes in Functional Connectivity among Prefrontal Cortical Neurons , 2007, The Journal of Neuroscience.

[62]  H. Schulz,et al.  Phasic or transient? Comment on the terminology of the AASM manual for the scoring of sleep and associated events. , 2007, Journal of clinical sleep medicine : JCSM : official publication of the American Academy of Sleep Medicine.

[63]  Parashkev Nachev,et al.  Space and the parietal cortex , 2007, Trends in Cognitive Sciences.

[64]  Justin L. Vincent,et al.  Intrinsic functional architecture in the anaesthetized monkey brain , 2007, Nature.

[65]  C. Shatz,et al.  A Burst-Based “Hebbian” Learning Rule at Retinogeniculate Synapses Links Retinal Waves to Activity-Dependent Refinement , 2007, PLoS biology.

[66]  Klaus Scheffler,et al.  Dissociated lateralization of transient and sustained blood oxygen level-dependent signal components in human primary auditory cortex , 2007, NeuroImage.

[67]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[68]  M. Corbetta,et al.  Electrophysiological signatures of resting state networks in the human brain , 2007, Proceedings of the National Academy of Sciences.

[69]  J. C. de Munck,et al.  Artifact removal in co-registered EEG/fMRI by selective average subtraction , 2007, Clinical Neurophysiology.

[70]  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 .

[71]  A. Marks,et al.  Associations between noise sensitivity and sleep, subjectively evaluated sleep quality, annoyance, and performance after exposure to nocturnal traffic noise. , 2007, Noise & health.

[72]  Abraham Z. Snyder,et al.  Moving GLM ballistocardiogram artifact reduction for EEG acquired simultaneously with fMRI , 2007, Clinical Neurophysiology.

[73]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[74]  S. Petersen,et al.  A dual-networks architecture of top-down control , 2008, Trends in Cognitive Sciences.

[75]  A. Braun,et al.  fMRI differences between early and late stage-1 sleep , 2008, Neuroscience Letters.

[76]  M. Fukunaga,et al.  Low frequency BOLD fluctuations during resting wakefulness and light sleep: A simultaneous EEG‐fMRI study , 2008, Human brain mapping.

[77]  Maolin Qiu,et al.  Spatial nonuniformity of the resting CBF and BOLD responses to sevoflurane: In vivo study of normal human subjects with magnetic resonance imaging , 2008, Human brain mapping.

[78]  M. Raichle,et al.  Resting states affect spontaneous BOLD oscillations in sensory and paralimbic cortex. , 2008, Journal of neurophysiology.

[79]  Learning to see in stereo , 2009, Nature Neuroscience.