Sleep debt elicits negative emotional reaction through diminished amygdala-anterior cingulate functional connectivity

• Published in: PloS one Vol. 8; no. 2; p. e56578
• Main Authors: Motomura, Yuki, Kitamura, Shingo, Oba, Kentaro, Terasawa, Yuri, Enomoto, Minori, Katayose, Yasuko, Hida, Akiko, Moriguchi, Yoshiya, Higuchi, Shigekazu, Mishima, Kazuo
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 13-02-2013; Public Library of Science (PLoS)
• Subjects: Adenosine; Adult; Affect - physiology; Amygdala; Amygdala - physiopathology; Anxiety; Anxiety - physiopathology; Anxiety - psychology; Behavior disorders; Biology; Brain; Brain mapping; Confusion - physiopathology; Confusion - psychology; Connectivity; Cortex (cingulate); Cross-Over Studies; Electroencephalography; Emotions; Facial Expression; Functional magnetic resonance imaging; Gyrus Cinguli - physiopathology; Homeostasis; Human error; Humans; Instability; Magnetic resonance; Magnetic Resonance Imaging; Male; Medical imaging; Medicine; Mental health; Mood; Neural networks; Neuroimaging; Neurology; Ocean energy resources; Polysomnography; Psychiatry; Psychomotor performance; Simulation; Sleep; Sleep - physiology; Sleep and wakefulness; Sleep deprivation; Sleep Deprivation - physiopathology; Sleep Deprivation - psychology; Sleepiness; Social and Behavioral Sciences; Stability; Studies; Surveys and Questionnaires; Wave power; Young Adult; Japan
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0056578

Sleep debt reportedly increases emotional instability, such as anxiety and confusion, in addition to sleepiness and psychomotor impairment. However, the neural basis of emotional instability due to sleep debt has yet to be elucidated. This study investigated changes in emotional responses that are elicited by the simulation of short-term sleep loss and the brain regions responsible for these changes.
Fourteen healthy adult men aged 24.1±3.3 years (range, 20-32 years) participated in a within-subject crossover study consisting of 5-day sessions of both sleep debt (4 h for time in bed) and sleep control (8 h for time in bed). On the last day of each session, participants underwent polysomnography and completed the State-Trait Anxiety Inventory and Profile of Mood States questionnaires. In addition, functional magnetic resonance imaging was conducted while performing an emotional face viewing task.
Restricted sleep over the 5-day period increased the activity of the left amygdala in response to the facial expression of fear, whereas a happy facial expression did not change the activity. Restricted sleep also resulted in a significant decrease in the functional connectivity between the amygdala and the ventral anterior cingulate cortex (vACC) in proportion to the degree of sleep debt (as indicated by the percentage of slow wave sleep and δ wave power). This decrease was significantly correlated with activation of the left amygdala and deterioration of subjective mood state.
The results of this study suggest that continuous and accumulating sleep debt that can be experienced in everyday life can downregulate the functional suppression of the amygdala by the vACC and consequently enhance the response of the amygdala to negative emotional stimuli. Such functional alteration in emotional control may, in part, be attributed to the neural basis of emotional instability during sleep debt.