Low frequency BOLD fluctuations during resting wakefulness and light sleep: A simultaneous EEG‐fMRI study

Recent blood oxygenation level dependent functional MRI (BOLD fMRI) studies of the human brain have shown that in the absence of external stimuli, activity persists in the form of distinct patterns of temporally correlated signal fluctuations. In this work, we investigated the spontaneous BOLD signal fluctuations during states of reduced consciousness such as drowsiness and sleep. For this purpose, we performed BOLD fMRI on normal subjects during varying levels of consciousness, from resting wakefulness to light (non‐slow wave) sleep. Depth of sleep was determined based on concurrently acquired EEG data. During light sleep, significant increases in the fluctuation level of the BOLD signal were observed in several cortical areas, among which visual cortex was the most significant. Correlations among brain regions involved with the default‐mode network persisted during light sleep. These results suggest that activity in areas such as the default‐mode network and primary sensory cortex, as measured from BOLD fMRI fluctuations, does not require a level of consciousness typical of wakefulness. Hum Brain Mapp, 2008. © 2007 Wiley‐Liss, Inc.

[1]  G. Moruzzi,et al.  Brain stem reticular formation and activation of the EEG. , 1949, Electroencephalography and clinical neurophysiology.

[2]  E. Evarts,et al.  Spontaneous Discharge of Single Neurons during Sleep and Waking , 1962, Science.

[3]  O D Creutzfeldt,et al.  Relations between EEG phenomena and potentials of single cortical cells. II. Spontaneous and convulsoid activity. , 1966, Electroencephalography and clinical neurophysiology.

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

[5]  L. DeLisi,et al.  The Genain quadruplets: Electrophysiological, positron emission, and x-ray tomographic studies , 1984, Psychiatry Research.

[6]  M. Mintun,et al.  Brain oxygen utilization measured with O-15 radiotracers and positron emission tomography. , 1984, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[7]  D. C. Howell Statistical Methods for Psychology , 1987 .

[8]  M. Mintun,et al.  Noninvasive functional brain mapping by change-distribution analysis of averaged PET images of H215O tissue activity. , 1989, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[9]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[10]  D. Heistad,et al.  Vasomotion of basilar arteries in vivo. , 1990, The American journal of physiology.

[11]  S. Ogawa Brain magnetic resonance imaging with contrast-dependent oxygenation , 1990 .

[12]  R. Turner,et al.  Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[13]  R J Roman,et al.  Spontaneous Flow Oscillations in the Cerebral Cortex during Acute Changes in Mean Arterial Pressure , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[14]  P. Maquet,et al.  Cerebral glucose utilization during stage 2 sleep in man , 1992, Brain Research.

[15]  R. S. Hinks,et al.  Time course EPI of human brain function during task activation , 1992, Magnetic resonance in medicine.

[16]  G. Moruzzi,et al.  Brain stem reticular formation and activation of the EEG. 1949. , 1995, The Journal of neuropsychiatry and clinical neurosciences.

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

[18]  C. Jones,et al.  Regulation of coronary blood flow: coordination of heterogeneous control mechanisms in vascular microdomains. , 1995, Cardiovascular research.

[19]  M. Hallett,et al.  Activation of the primary visual cortex by Braille reading in blind subjects , 1996, Nature.

[20]  J D Watson,et al.  Nonparametric Analysis of Statistic Images from Functional Mapping Experiments , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[21]  A. Grinvald,et al.  Dynamics of Ongoing Activity: Explanation of the Large Variability in Evoked Cortical Responses , 1996, Science.

[22]  Philip McGuire,et al.  Brain activity during stimulus independent thought. , 1996 .

[23]  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.

[24]  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.

[25]  P. Mitra,et al.  The nature of spatiotemporal changes in cerebral hemodynamics as manifested in functional magnetic resonance imaging , 1997, Magnetic resonance in medicine.

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

[27]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: I. Increases in Subcortical Structures and Cerebellum but Not in Nonvisual Cortex , 1997, Journal of Cognitive Neuroscience.

[28]  M. Lowe,et al.  Functional Connectivity in Single and Multislice Echoplanar Imaging Using Resting-State Fluctuations , 1998, NeuroImage.

[29]  Y Yonekura,et al.  Neural networks for generation and suppression of alpha rhythm: a PET study , 1998, Neuroreport.

[30]  H. Onoe,et al.  Brain Networks Affected by Synchronized Sleep Visualized by Positron Emission Tomography , 1998, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[31]  J. A. Frost,et al.  Conceptual Processing during the Conscious Resting State: A Functional MRI Study , 1999, Journal of Cognitive Neuroscience.

[32]  John Suckling,et al.  Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain , 1999, IEEE Transactions on Medical Imaging.

[33]  Masanori Sekimoto,et al.  Activity of Midbrain Reticular Formation and Neocortex during the Progression of Human Non-Rapid Eye Movement Sleep , 1999, The Journal of Neuroscience.

[34]  V. Haughton,et al.  Mapping functionally related regions of brain with functional connectivity MR imaging. , 2000, AJNR. American journal of neuroradiology.

[35]  M E Meyerand,et al.  Combining independent component analysis and correlation analysis to probe interregional connectivity in fMRI task activation datasets. , 2000, Magnetic resonance imaging.

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

[37]  Robert Turner,et al.  A Method for Removing Imaging Artifact from Continuous EEG Recorded during Functional MRI , 2000, NeuroImage.

[38]  J. Lurito,et al.  Correlations in Low-Frequency BOLD Fluctuations Reflect Cortico-Cortical Connections , 2000, NeuroImage.

[39]  A. Villringer,et al.  Spontaneous Low Frequency Oscillations of Cerebral Hemodynamics and Metabolism in Human Adults , 2000, NeuroImage.

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

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

[42]  S Laureys,et al.  Sleeping brain, learning brain. The role of sleep for memory systems , 2001, Neuroreport.

[43]  B. Mazoyer,et al.  Cortical networks for working memory and executive functions sustain the conscious resting state in man , 2001, Brain Research Bulletin.

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

[45]  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.

[46]  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.

[47]  P. Skudlarski,et al.  Detection of functional connectivity using temporal correlations in MR images , 2002, Human brain mapping.

[48]  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.

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

[50]  Mark S. Cohen,et al.  Simultaneous EEG and fMRI of the alpha rhythm , 2002, Neuroreport.

[51]  Peter Kellman,et al.  Application of sensitivity‐encoded echo‐planar imaging for blood oxygen level‐dependent functional brain imaging † , 2002, Magnetic resonance in medicine.

[52]  Hellmuth Obrig,et al.  Correlates of alpha rhythm in functional magnetic resonance imaging and near infrared spectroscopy , 2003, NeuroImage.

[53]  Andreas Kleinschmidt,et al.  EEG-correlated fMRI of human alpha activity , 2003, NeuroImage.

[54]  N. Logothetis,et al.  Very slow activity fluctuations in monkey visual cortex: implications for functional brain imaging. , 2003, Cerebral cortex.

[55]  Irene Tracey,et al.  Resting fluctuations in arterial carbon dioxide induce significant low frequency variations in BOLD signal , 2004, NeuroImage.

[56]  E. Formisano,et al.  Functional connectivity as revealed by spatial independent component analysis of fMRI measurements during rest , 2004, Human brain mapping.

[57]  Renxin Chu,et al.  Magnetic Resonance in Medicine 51:22–26 (2004) Signal-to-Noise Ratio and Parallel Imaging Performance of a 16-Channel Receive-Only Brain Coil Array at , 2022 .

[58]  T. Uema,et al.  Deactivation by benzodiazepine of the basal forebrain and amygdala in normal humans during sleep: a placebo-controlled [15O]H2O PET study. , 2004, The American journal of psychiatry.

[59]  M. J. Meloy,et al.  The neural basis of the psychomotor vigilance task. , 2005, Sleep.

[60]  H. Berger Über das Elektrenkephalogramm des Menschen , 1929, Archiv für Psychiatrie und Nervenkrankheiten.

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

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

[63]  Gang Chen,et al.  Functional imaging analysis contest (FIAC) analysis according to AFNI and SUMA , 2006, Human brain mapping.

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

[65]  P. Fransson How default is the default mode of brain function? Further evidence from intrinsic BOLD signal fluctuations , 2006, Neuropsychologia.

[66]  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.

[67]  Helmut Laufs,et al.  Where the BOLD signal goes when alpha EEG leaves , 2006, NeuroImage.

[68]  Yehezkel Yeshurun,et al.  Widespread functional connectivity and fMRI fluctuations in human visual cortex in the absence of visual stimulation , 2006, NeuroImage.

[69]  Stephen M. Smith,et al.  fMRI resting state networks define distinct modes of long-distance interactions in the human brain , 2006, NeuroImage.

[70]  Marcus E Raichle,et al.  Neuroscience. The brain's dark energy. , 2006, Science.

[71]  Thomas E. Nichols,et al.  Non-white noise in fMRI: Does modelling have an impact? , 2006, NeuroImage.

[72]  M. Raichle The Brain's Dark Energy , 2006, Science.