Sleep Deprivation Impairs the Human Central and Peripheral Nervous System Discrimination of Social Threat
Adult
Central Nervous System
Male
Time Factors
social threat
Adolescent
1.1 Normal biological development and functioning
Image Processing
Polysomnography
Emotions
emotion
Basic Behavioral and Social Science
anterior insula
Medical and Health Sciences
Mass Spectrometry
Perceptual Disorders
Young Adult
03 medical and health sciences
Computer-Assisted
0302 clinical medicine
Clinical Research
Underpinning research
Heart Rate
Behavioral and Social Science
Peripheral Nervous System
Image Processing, Computer-Assisted
Humans
10. No inequality
Neurology & Neurosurgery
Psychology and Cognitive Sciences
Neurosciences
Electroencephalography
amygdala
sleep deprivation
Magnetic Resonance Imaging
Oxygen
anterior cingulate cortex
Mental Health
13. Climate action
Sleep Deprivation
Female
Sleep Research
Photic Stimulation
DOI:
10.1523/jneurosci.5254-14.2015
Publication Date:
2015-07-15T17:00:29Z
AUTHORS (4)
ABSTRACT
Facial expressions represent one of the most salient cues in our environment. They communicate the affective state and intent of an individual and, if interpreted correctly, adaptively influence the behavior of others in return. Processing of such affective stimuli is known to require reciprocal signaling between central viscerosensory brain regions and peripheral-autonomic body systems, culminating in accurate emotion discrimination. Despite emerging links between sleep and affective regulation, the impact of sleep loss on the discrimination of complex social emotions within and between the CNS and PNS remains unknown. Here, we demonstrate in humans that sleep deprivation impairs both viscerosensory brain (anterior insula, anterior cingulate cortex, amygdala) and autonomic-cardiac discrimination of threatening from affiliative facial cues. Moreover, sleep deprivation significantly degrades the normally reciprocal associations between these central and peripheral emotion-signaling systems, most prominent at the level of cardiac-amygdala coupling. In addition, REM sleep physiology across the sleep-rested night significantly predicts the next-day success of emotional discrimination within this viscerosensory network across individuals, suggesting a role for REM sleep in affective brain recalibration. Together, these findings establish that sleep deprivation compromises the faithful signaling of, and the "embodied" reciprocity between, viscerosensory brain and peripheral autonomic body processing of complex social signals. Such impairments hold ecological relevance in professional contexts in which the need for accurate interpretation of social cues is paramount yet insufficient sleep is pervasive.
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