fMRI evidence for multisensory recruitment associated with rapid eye movements during sleep

Authors

  • Charles Chong-Hwa Hong,

    Corresponding author
    1. Department of Psychiatry and Behavioral Sciences, Johns Hopkins University, Baltimore, Maryland
    • F. M. Kirby Research Center for Functional Brain Imaging, Kennedy Krieger Institute, 707 North Broadway, Baltimore, Maryland 21205, USA
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  • James C. Harris,

    1. Department of Psychiatry and Behavioral Sciences, Johns Hopkins University, Baltimore, Maryland
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  • Godfrey D. Pearlson,

    1. Department of Psychiatry and Behavioral Sciences, Johns Hopkins University, Baltimore, Maryland
    2. Olin Neuropsychiatry Research Center, Institute of Living, Hartford Hospital, Connecticut
    3. Department of Psychiatry, Yale University, New Haven, Connecticut
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  • Jin-Suh Kim,

    1. Department of Psychiatry and Behavioral Sciences, Johns Hopkins University, Baltimore, Maryland
    2. Olin Neuropsychiatry Research Center, Institute of Living, Hartford Hospital, Connecticut
    3. Department of Psychiatry, Yale University, New Haven, Connecticut
    Current affiliation:
    1. Department of Radiology, University of Iowa, Iowa 52242, USA
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  • Vince D. Calhoun,

    1. Department of Psychiatry and Behavioral Sciences, Johns Hopkins University, Baltimore, Maryland
    2. Olin Neuropsychiatry Research Center, Institute of Living, Hartford Hospital, Connecticut
    3. Department of Psychiatry, Yale University, New Haven, Connecticut
    Current affiliation:
    1. The MIND Institute, 1101 Yale Boulevard, Albuquerque, NM 87131, USA and Department of ECE, University of New Mexico, Albuquerque, NM 87131, USA
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  • James H. Fallon,

    1. Department of Anatomy and Neurobiology, University of California, Irvine, California
    2. Brain Imaging Center, Department of Psychiatry and Human Behavior, University of California, Irvine, California
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  • Xavier Golay,

    1. Department of Radiology, Johns Hopkins University, Baltimore, Maryland
    2. F. M. Kirby Research Center, Kennedy Krieger Institute, Baltimore, Maryland
    Current affiliation:
    1. Laboratory of Molecular Imaging, Singapore Bioimaging Consortium, Singapore 138667
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  • Joseph S. Gillen,

    1. Department of Radiology, Johns Hopkins University, Baltimore, Maryland
    2. F. M. Kirby Research Center, Kennedy Krieger Institute, Baltimore, Maryland
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  • Daniel J. Simmonds,

    1. Department of Developmental Cognitive Neurology, Kennedy Krieger Institute, Baltimore, Maryland
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  • Peter C.M. van Zijl,

    1. Department of Radiology, Johns Hopkins University, Baltimore, Maryland
    2. F. M. Kirby Research Center, Kennedy Krieger Institute, Baltimore, Maryland
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  • David S. Zee,

    1. Department of Neurology, Johns Hopkins University, Baltimore, Maryland
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  • James J. Pekar

    1. Department of Radiology, Johns Hopkins University, Baltimore, Maryland
    2. F. M. Kirby Research Center, Kennedy Krieger Institute, Baltimore, Maryland
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Abstract

We studied the neural correlates of rapid eye movement during sleep (REM) by timing REMs from video recording and using rapid event-related functional MRI. Consistent with the hypothesis that REMs share the brain systems and mechanisms with waking eye movements and are visually-targeted saccades, we found REM-locked activation in the primary visual cortex, thalamic reticular nucleus (TRN), ‘visual claustrum’, retrosplenial cortex (RSC, only on the right hemisphere), fusiform gyrus, anterior cingulate cortex, and the oculomotor circuit that controls awake saccadic eye movements (and subserves awake visuospatial attention). Unexpectedly, robust activation also occurred in non-visual sensory cortices, motor cortex, language areas, and the ascending reticular activating system, including basal forebrain, the major source of cholinergic input to the entire cortex. REM-associated activation of these areas, especially non-visual primary sensory cortices, TRN and claustrum, parallels findings from waking studies on the interactions between multiple sensory data, and their ‘binding’ into a unified percept, suggesting that these mechanisms are also shared in waking and dreaming and that the sharing goes beyond the expected visual scanning mechanisms. Surprisingly, REMs were associated with a decrease in signal in specific periventricular subregions, matching the distribution of the serotonergic supraependymal plexus. REMs might serve as a useful task-free probe into major brain systems for functional brain imaging. Hum Brain Mapp 2009. © 2008 Wiley-Liss, Inc.

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