Connectivity pattern changes in default-mode network with deep non-REM and REM sleep

Recent studies have compared default-mode network (DMN) connectivity in different arousal levels to investigate the relationship between consciousness and DMN. The comparison between the DMN in rapid eye movement (REM) sleep with that in non-REM (NREM) sleep is useful for revealing the relationship between arousal level and DMN, because the arousal level is at its lowest during deep NREM, while during REM sleep it is as high as wakefulness. Functional magnetic resonance imaging (fMRI) and polysomnogram data were acquired from participants in REM, deep NREM, and light NREM sleep, and the DMN was compared using functional connectivity analysis. Our analysis revealed that functional connectivity among the DMN core regions - the posterior cingulate cortex, rostral anterior cingulate cortex, and inferior parietal lobule - remained consistent across sleep states. In contrast, connectivity involving the DMN subsystems of REM sleep differs from that of NREM sleep, and the change well accounts for the characteristics of REM sleep. Our results suggest that both the DMN core region and subsystems may not relate to the maintenance of arousal. The DMN core network and subsystems may respectively serve to integrate brain regions and perform function specific to each level of arousal.

[1]  R. Buckner,et al.  Functional-Anatomic Fractionation of the Brain's Default Network , 2010, Neuron.

[2]  Keith A. Johnson,et al.  Cortical Hubs Revealed by Intrinsic Functional Connectivity: Mapping, Assessment of Stability, and Relation to Alzheimer's Disease , 2009, The Journal of Neuroscience.

[3]  D Lehmann,et al.  Sleep deprivation: effect on sleep stages and EEG power density in man. , 1981, Electroencephalography and clinical neurophysiology.

[4]  E. Stein,et al.  Cingulate activation increases dynamically with response speed under stimulus unpredictability. , 2007, Cerebral cortex.

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

[6]  Yong He,et al.  Functional connectivity between the thalamus and visual cortex under eyes closed and eyes open conditions: A resting‐state fMRI study , 2009, Human brain mapping.

[7]  H. Barbas,et al.  Medial Prefrontal Cortices Are Unified by Common Connections With Superior Temporal Cortices and Distinguished by Input From Memory‐Related Areas in the Rhesus Monkey , 1999, The Journal of comparative neurology.

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

[9]  W. Singer Consciousness and the Binding Problem , 2001, Annals of the New York Academy of Sciences.

[10]  M. Greicius,et al.  Persistent default‐mode network connectivity during light sedation , 2008, Human brain mapping.

[11]  Alexander A. Borbély,et al.  The effect of 3-h and 6-h sleep deprivation on sleep and EEG spectra of the rat , 1990, Behavioural Brain Research.

[12]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[13]  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.

[14]  C J Price,et al.  The neural systems sustaining face and proper-name processing. , 1998, Brain : a journal of neurology.

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

[16]  C. N. Macrae,et al.  Finding the Self? An Event-Related fMRI Study , 2002, Journal of Cognitive Neuroscience.

[17]  G. Edelman,et al.  Consciousness and Complexity , 1998 .

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

[19]  C. Degueldre,et al.  Functional neuroanatomy of human rapid-eye-movement sleep and dreaming , 1996, Nature.

[20]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[21]  M. D’Esposito,et al.  Is the rostro-caudal axis of the frontal lobe hierarchical? , 2009, Nature Reviews Neuroscience.

[22]  F. Varela,et al.  Perception's shadow: long-distance synchronization of human brain activity , 1999, Nature.

[23]  Biyu J. He,et al.  Electrophysiological correlates of the brain's intrinsic large-scale functional architecture , 2008, Proceedings of the National Academy of Sciences.

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

[25]  B. Levine,et al.  The functional neuroanatomy of autobiographical memory: A meta-analysis , 2006, Neuropsychologia.

[26]  R. Stickgold,et al.  Dreaming and the brain: Toward a cognitive neuroscience of conscious states , 2000, Behavioral and Brain Sciences.

[27]  Seung-Schik Yoo,et al.  The Unrested Resting Brain: Sleep Deprivation Alters Activity within the Default-mode Network , 2010, Journal of Cognitive Neuroscience.

[28]  R Stickgold,et al.  Brain-Mind States: Reciprocal Variation in Thoughts and Hallucinations , 2001, Psychological science.

[29]  Sterling C. Johnson,et al.  Neural correlates of self-evaluative accuracy after traumatic brain injury , 2006, Neuropsychologia.

[30]  Kevin Murphy,et al.  The impact of global signal regression on resting state correlations: Are anti-correlated networks introduced? , 2009, NeuroImage.

[31]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

[33]  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.

[34]  R. Stickgold,et al.  The neuropsychology of REM sleep dreaming. , 1998, Neuroreport.

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

[36]  C. Frith,et al.  Interacting minds--a biological basis. , 1999, Science.

[37]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

[38]  M. Fox,et al.  The global signal and observed anticorrelated resting state brain networks. , 2009, Journal of neurophysiology.

[39]  R. Llinás,et al.  Coherent 40-Hz oscillation characterizes dream state in humans. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[40]  V. Natale,et al.  Slow wave sleep dreaming. , 1992, Sleep.

[41]  C. Gross,et al.  Representations of faces and body parts in macaque temporal cortex: a functional MRI study. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[42]  M. Buonocore,et al.  Remembering familiar people: the posterior cingulate cortex and autobiographical memory retrieval , 2001, Neuroscience.

[43]  G. Tononi,et al.  Consciousness and Anesthesia , 2008, Science.

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

[45]  P. Skudlarski,et al.  Brain Connectivity Is Not Only Lower but Different in Schizophrenia: A Combined Anatomical and Functional Approach , 2010, Biological Psychiatry.

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

[47]  D. Leopold,et al.  Neuronal correlates of spontaneous fluctuations in fMRI signals in monkey visual cortex: Implications for functional connectivity at rest , 2008, Human brain mapping.

[48]  Scott T. Grafton,et al.  Wandering Minds: The Default Network and Stimulus-Independent Thought , 2007, Science.

[49]  A. Rechtschaffen A manual of standardized terminology, techniques and scoring system for sleep of human subjects , 1968 .

[50]  L. Fellows,et al.  Dorsal Medial Prefrontal Cortex Plays a Necessary Role in Rapid Error Prediction in Humans , 2008, The Journal of Neuroscience.

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

[52]  S Laureys,et al.  Intrinsic Brain Activity in Altered States of Consciousness , 2008, Annals of the New York Academy of Sciences.

[53]  V. Haughton,et al.  Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. , 2001, AJNR. American journal of neuroradiology.

[54]  Christian Degueldre,et al.  Functional Neuroanatomy of Human Slow Wave Sleep , 1997, The Journal of Neuroscience.

[55]  Rajesh Kumar,et al.  A method for removal of global effects from fMRI time series , 2004, NeuroImage.

[56]  Jordan Grafman,et al.  The medial prefrontal cortex mediates social event knowledge , 2009, Trends in Cognitive Sciences.

[57]  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.