Sleep Debt Elicits Negative Emotional Reaction through Diminished Amygdala-Anterior Cingulate Functional Connectivity

Yuki Motomura, Shingo Kitamura, Kentaro Oba, Yuuri Terasawa, Minori Enomoto, Yasuko Katayose, Akiko Hida, Yoshiya Moriguchi, Shigekazu Higuchi, Kazuo Mishima

Research output: Contribution to journalArticle

79 Citations (Scopus)

Abstract

Objectives: 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. Subjects and Methods: 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. Results: 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. Conclusion: 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.

Original languageEnglish
Article numbere56578
JournalPLoS One
Volume8
Issue number2
DOIs
Publication statusPublished - 2013 Feb 13
Externally publishedYes

Fingerprint

debt
amygdala
Gyrus Cinguli
Amygdala
sleep
Sleep
Facial Expression
anxiety
emotions
cortex
Anxiety
Psychomotor Disorders
Confusion
Wave power
Polysomnography
fearfulness
magnetic resonance imaging
Cross-Over Studies
Fear
Deterioration

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Sleep Debt Elicits Negative Emotional Reaction through Diminished Amygdala-Anterior Cingulate Functional Connectivity. / Motomura, Yuki; Kitamura, Shingo; Oba, Kentaro; Terasawa, Yuuri; Enomoto, Minori; Katayose, Yasuko; Hida, Akiko; Moriguchi, Yoshiya; Higuchi, Shigekazu; Mishima, Kazuo.

In: PLoS One, Vol. 8, No. 2, e56578, 13.02.2013.

Research output: Contribution to journalArticle

Motomura, Y, Kitamura, S, Oba, K, Terasawa, Y, Enomoto, M, Katayose, Y, Hida, A, Moriguchi, Y, Higuchi, S & Mishima, K 2013, 'Sleep Debt Elicits Negative Emotional Reaction through Diminished Amygdala-Anterior Cingulate Functional Connectivity', PLoS One, vol. 8, no. 2, e56578. https://doi.org/10.1371/journal.pone.0056578
Motomura, Yuki ; Kitamura, Shingo ; Oba, Kentaro ; Terasawa, Yuuri ; Enomoto, Minori ; Katayose, Yasuko ; Hida, Akiko ; Moriguchi, Yoshiya ; Higuchi, Shigekazu ; Mishima, Kazuo. / Sleep Debt Elicits Negative Emotional Reaction through Diminished Amygdala-Anterior Cingulate Functional Connectivity. In: PLoS One. 2013 ; Vol. 8, No. 2.
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