Altered Processing of Acoustic Stimuli during Sleep: Reduced Auditory Activation and Visual Deactivation Detected by a Combined fMRI/EEG Study

Although there is evidence that acoustic stimuli are processed differently during sleep and wakefulness, little is known about the underlying neuronal mechanisms. In the present study, the processing of an acoustic stimulus was investigated during different non rapid eye movement (NREM) sleep stages using a combined EEG/fMRI approach in healthy human volunteers: A text stimulus was presented to sleep-deprived subjects prior to and after the onset of sleep, and single-slice silent fMRI were acquired. We found significantly different blood oxygenation level-dependent (BOLD) contrast responses during sleep compared to wakefulness. During NREM sleep stages 1 and 2 and during slow wave sleep (SWS) we observed reduced activation in the auditory cortex and a pronounced negative signal in the visual cortex and precuneus. Acoustic stimulation during sleep was accompanied by an increase in EEG frequency components in the low delta frequency range. Provided that neurovascular coupling is not altered during sleep, the negative transmodal BOLD response which is most pronounced during NREM sleep stages 1 and 2 reflects a deactivation predominantly in the visual cortex suggesting that this decrease in neuronal activity protects the brain from the arousing effects of external stimulation during sleep not only in the primary targeted sensory cortex but also in other brain regions.

[1]  Tarek A. Yousry,et al.  Cortical deactivation during vestibular and nociceptive galvanic stimulation (fMRI) , 2000, NeuroImage.

[2]  M Steriade,et al.  Electrophysiological correlates of sleep delta waves. , 1998, Electroencephalography and clinical neurophysiology.

[3]  D. Somers,et al.  Functional MRI reveals spatially specific attentional modulation in human primary visual cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[4]  François Mauguière,et al.  A differential brain response to the subject's own name persists during sleep , 1999, Clinical Neurophysiology.

[5]  M. Corbetta,et al.  Top-down modulation of early sensory cortex. , 1997 .

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

[7]  T. Brandt,et al.  Reciprocal inhibitory visual-vestibular interaction. Visual motion stimulation deactivates the parieto-insular vestibular cortex. , 1998, Brain : a journal of neurology.

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

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

[10]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[11]  C Gössl,et al.  Dynamic models in fMRI , 2000, Magnetic resonance in medicine.

[12]  John C. Gore,et al.  ROC Analysis of Statistical Methods Used in Functional MRI: Individual Subjects , 1999, NeuroImage.

[13]  A. Shmuel,et al.  Negative BOLD response and its coupling to the positive response in the human brain , 2001, NeuroImage.

[14]  K. Carlsson,et al.  Tickling Expectations: Neural Processing in Anticipation of a Sensory Stimulus , 2000, Journal of Cognitive Neuroscience.

[15]  M. Raichle,et al.  Blood flow changes in human somatosensory cortex during anticipated stimulation , 1995, Nature.

[16]  Egill Rostrup,et al.  Change of visually induced cortical activation patterns during development , 1996, The Lancet.

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

[18]  R R Edelman,et al.  Silent functional magnetic resonance imaging demonstrates focal activation in rapid eye movement sleep , 1999, Neurology.

[19]  Alfred L. Loomis,et al.  DISTRIBUTION OF DISTURBANCE-PATTERNS IN THE HUMAN ELECTROENCEPHALOGRAM, WITH SPECIAL REFERENCE TO SLEEP , 1938 .

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

[21]  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.

[22]  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.

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

[24]  Alexander M. Harner,et al.  Task-dependent influences of attention on the activation of human primary visual cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Juergen Hennig,et al.  Visual Processing in Infants and Children Studied Using Functional MRI , 1999, Pediatric Research.