Decreased connectivity between the thalamus and the neocortex during human nonrapid eye movement sleep.
OBJECTIVE
To determine whether thalamocortical signaling between the thalamus and the neocortex decreases from wakefulness to nonrapid eye movement (NREM) sleep.


METHODS
Electroencephalography and functional magnetic resonance imaging data were collected simultaneously at 02:30 after 44 h of sleep deprivation.


METHODS
Clinical research hospital.


METHODS
There were six volunteers (mean age 24.2 y, one male) who yielded sufficient amounts of usable, artifact-free data. All were healthy, right-handed native English speakers who consumed less than 710 mL of caffeinated beverages per day. Psychiatric, neurological, circadian, and sleep disorders were ruled out by reviewing each patient's clinical history. A standard clinical nocturnal polysomnogram was negative for sleep disorders.


METHODS
N/A.


RESULTS
A functional connectivity analysis was performed using the centromedian nucleus as the seed region. We determined the statistical significance of the difference between correlations obtained during wakefulness and during slow wave sleep. Neocortical regions displaying decreased thalamic connectivity were all heteromodal regions (e.g., medial frontal gyrus and posterior cingulate/precuneus), whereas there was a complete absence of neocortical regions displaying increased thalamic connectivity. Although more clusters of significant decreases were observed in stage 2 sleep, these results were similar to the results for slow wave sleep.


CONCLUSIONS
Results of this study provide evidence of a functional deafferentation of the neocortex during nonrapid eye movement (NREM) sleep in humans. This deafferentation likely accounts for increased sensory awareness thresholds during NREM sleep. Decreased thalamocortical connectivity in regions such as the posterior cingulate/precuneus also are observed in coma and general anesthesia, suggesting that changes in thalamocortical connectivity may act as a universal "control switch" for changes in consciousness that are observed in coma, general anesthesia, and natural sleep.
Behavioral Biology Branch, Walter Reed Army Institute of Research, Silver Spring, MD.
Dante
D
Picchioni
Behavioral Biology Branch, Walter Reed Army Institute of Research, Silver Spring, MD ; Computer Systems Laboratory, Thomas Jefferson High School for Science and Technology, Alexandria, VA.
Morgan L
ML
Pixa
Advanced MRI Section, National Institute of Neurological Disorders and Stroke, Bethesda, MD.
Masaki
M
Fukunaga
Language Section, National Institute on Deafness and Other Communication Disorders, Bethesda, MD.
Walter S
WS
Carr
Advanced MRI Section, National Institute of Neurological Disorders and Stroke, Bethesda, MD.
Silvina G
SG
Horovitz
Language Section, National Institute on Deafness and Other Communication Disorders, Bethesda, MD.
Allen R
AR
Braun
Advanced MRI Section, National Institute of Neurological Disorders and Stroke, Bethesda, MD.
Jeff H
JH
Duyn
D004569:Electroencephalography; D005133:Eye Movements / Q000502:physiology*; D005260:Female; D064368:Healthy Volunteers; D006801:Humans; D008279:Magnetic Resonance Imaging; D008297:Male; D019579:Neocortex / Q000502:physiology*; D017286:Polysomnography; D012892:Sleep Deprivation; D012894:Sleep Stages / Q000502:physiology*; D013788:Thalamus / Q000502:physiology*; D014851:Wakefulness / Q000502:physiology; D055815:Young Adult
Electroencephalography; functional connectivity; functional magnetic resonance imaging; neocortex; nonspecific nuclei; sleep; thalamus