Sleepiness induced by sleep-debt enhanced amygdala activity for subliminal signals of fear

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

13 Citations (Scopus)

Abstract

Background: Emotional information is frequently processed below the level of consciousness, where subcortical regions of the brain are thought to play an important role. In the absence of conscious visual experience, patients with visual cortex damage discriminate the valence of emotional expression. Even in healthy individuals, a subliminal mechanism can be utilized to compensate for a functional decline in visual cognition of various causes such as strong sleepiness. In this study, sleep deprivation was simulated in healthy individuals to investigate functional alterations in the subliminal processing of emotional information caused by reduced conscious visual cognition and attention due to an increase in subjective sleepiness. Fourteen healthy adult men participated in a within-subject crossover study consisting of a 5-day session of sleep debt (SD, 4-h sleep) and a 5-day session of sleep control (SC, 8-h sleep). On the last day of each session, participants performed an emotional face-viewing task that included backward masking of nonconscious presentations during magnetic resonance scanning. Results: Finally, data from eleven participants who were unaware of nonconscious face presentations were analyzed. In fear contrasts, subjective sleepiness was significantly positively correlated with activity in the amygdala, ventromedial prefrontal cortex, hippocampus, and insular cortex, and was significantly negatively correlated with the secondary and tertiary visual areas and the fusiform face area. In fear-neutral contrasts, subjective sleepiness was significantly positively correlated with activity of the bilateral amygdala. Further, changes in subjective sleepiness (the difference between the SC and SD sessions) were correlated with both changes in amygdala activity and functional connectivity between the amygdala and superior colliculus in response to subliminal fearful faces.Conclusion: Sleepiness induced functional decline in the brain areas involved in conscious visual cognition of facial expressions, but also enhanced subliminal emotional processing via superior colliculus as represented by activity in the amygdala. These findings suggest that an evolutionally old and auxiliary subliminal hazard perception system is activated as a compensatory mechanism when conscious visual cognition is impaired. In addition, enhancement of subliminal emotional processing might cause involuntary emotional instability during sleep debt through changes in emotional response to or emotional evaluation of external stimuli.

Original languageEnglish
Article number97
JournalBMC Neuroscience
Volume15
Issue number1
DOIs
Publication statusPublished - 2014 Aug 19

Fingerprint

Amygdala
Fear
Sleep
Cognition
Superior Colliculi
Subliminal Stimulation
Facial Expression
Sleep Deprivation
Brain
Visual Cortex
Prefrontal Cortex
Consciousness
Automatic Data Processing
Cerebral Cortex
Cross-Over Studies
Hippocampus
Magnetic Resonance Spectroscopy

Keywords

  • Amygdala
  • Emotion
  • Fearful face
  • Nonconscious
  • Sleepiness
  • Subliminal
  • Unconscious

ASJC Scopus subject areas

  • Neuroscience(all)
  • Cellular and Molecular Neuroscience
  • Medicine(all)

Cite this

Sleepiness induced by sleep-debt enhanced amygdala activity for subliminal signals of fear. / Motomura, Yuki; Kitamura, Shingo; Oba, Kentaro; Terasawa, Yuuri; Enomoto, Minori; Katayose, Yasuko; Hida, Akiko; Moriguchi, Yoshiya; Higuchi, Shigekazu; Mishima, Kazuo.

In: BMC Neuroscience, Vol. 15, No. 1, 97, 19.08.2014.

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 2014, 'Sleepiness induced by sleep-debt enhanced amygdala activity for subliminal signals of fear', BMC Neuroscience, vol. 15, no. 1, 97. https://doi.org/10.1186/1471-2202-15-97
Motomura, Yuki ; Kitamura, Shingo ; Oba, Kentaro ; Terasawa, Yuuri ; Enomoto, Minori ; Katayose, Yasuko ; Hida, Akiko ; Moriguchi, Yoshiya ; Higuchi, Shigekazu ; Mishima, Kazuo. / Sleepiness induced by sleep-debt enhanced amygdala activity for subliminal signals of fear. In: BMC Neuroscience. 2014 ; Vol. 15, No. 1.
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abstract = "Background: Emotional information is frequently processed below the level of consciousness, where subcortical regions of the brain are thought to play an important role. In the absence of conscious visual experience, patients with visual cortex damage discriminate the valence of emotional expression. Even in healthy individuals, a subliminal mechanism can be utilized to compensate for a functional decline in visual cognition of various causes such as strong sleepiness. In this study, sleep deprivation was simulated in healthy individuals to investigate functional alterations in the subliminal processing of emotional information caused by reduced conscious visual cognition and attention due to an increase in subjective sleepiness. Fourteen healthy adult men participated in a within-subject crossover study consisting of a 5-day session of sleep debt (SD, 4-h sleep) and a 5-day session of sleep control (SC, 8-h sleep). On the last day of each session, participants performed an emotional face-viewing task that included backward masking of nonconscious presentations during magnetic resonance scanning. Results: Finally, data from eleven participants who were unaware of nonconscious face presentations were analyzed. In fear contrasts, subjective sleepiness was significantly positively correlated with activity in the amygdala, ventromedial prefrontal cortex, hippocampus, and insular cortex, and was significantly negatively correlated with the secondary and tertiary visual areas and the fusiform face area. In fear-neutral contrasts, subjective sleepiness was significantly positively correlated with activity of the bilateral amygdala. Further, changes in subjective sleepiness (the difference between the SC and SD sessions) were correlated with both changes in amygdala activity and functional connectivity between the amygdala and superior colliculus in response to subliminal fearful faces.Conclusion: Sleepiness induced functional decline in the brain areas involved in conscious visual cognition of facial expressions, but also enhanced subliminal emotional processing via superior colliculus as represented by activity in the amygdala. These findings suggest that an evolutionally old and auxiliary subliminal hazard perception system is activated as a compensatory mechanism when conscious visual cognition is impaired. In addition, enhancement of subliminal emotional processing might cause involuntary emotional instability during sleep debt through changes in emotional response to or emotional evaluation of external stimuli.",
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