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

Motomura, Yuki; Kitamura, Shingo; Oba, Kentaro; Terasawa, Yuri; Enomoto, Minori; Katayose, Yasuko; Hida, Akiko; Moriguchi, Yoshiya; Higuchi, Shigekazu; Mishima, Kazuo
February 2013
PLoS ONE;Feb2013, Vol. 8 Issue 2, p1
Academic Journal
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.


Related Articles

  • Underconnectivity of the superior temporal sulcus predicts emotion recognition deficits in autism. Alaerts, Kaat; Woolley, Daniel G.; Steyaert, Jean; Di Martino, Adriana; Swinnen, Stephan P.; Wenderoth, Nicole // Social Cognitive & Affective Neuroscience;Oct2014, Vol. 9 Issue 10, p1589 

    Neurodevelopmental disconnections have been assumed to cause behavioral alterations in autism spectrum disorders (ASDs). Here, we combined measurements of intrinsic functional connectivity (iFC) from resting-state functional magnetic resonance imaging (fMRI) with task-based fMRI to explore...

  • COMT Val158Met genotypes differentially influence subgenual cingulate functional connectivity in healthy females. Baeken, Chris; Marinazzo, Daniele; Claes, Stephan; Guo-Rong Wu; Van Schuerbeek, Peter; De Mey, Johan; Luypaert, Robert; De Raedt, Rudi // Frontiers in Human Neuroscience;Jun2014, Vol. 8, p1 

    Brain imaging studies have consistently shown subgenual Anterior Cingulate Cortical (sgACC) involvement in emotion processing. catechol-O-methyltransferase (COMT) Val158 and Met158 polymorphisms may influence such emotional brain processes in specific ways. Given that resting-state fMRI (rsfMRI)...

  • Voluntary Enhancement of Neural Signatures of Affiliative Emotion Using fMRI Neurofeedback. Moll, Jorge; Weingartner, Julie H.; Bado, Patricia; Basilio, Rodrigo; Sato, João R.; Melo, Bruno R.; Bramati, Ivanei E.; de Oliveira-Souza, Ricardo; Zahn, Roland // PLoS ONE;May2014, Vol. 9 Issue 5, p1 

    In Ridley Scott’s film “Blade Runner”, empathy-detection devices are employed to measure affiliative emotions. Despite recent neurocomputational advances, it is unknown whether brain signatures of affiliative emotions, such as tenderness/affection, can be decoded and...

  • Abnormal Functional Connectivity of Amygdala in Late-Onset Depression Was Associated with Cognitive Deficits. Yue, Yingying; Yuan, Yonggui; Hou, Zhenghua; Jiang, Wenhao; Bai, Feng; Zhang, Zhijun // PLoS ONE;Sep2013, Vol. 8 Issue 9, p1 

    Background: Major depressive disorder (MDD) is associated with decreased function of cortico-limbic circuits, which play important roles in the pathogenesis of MDD. Abnormal functional connectivity (FC) with the amygdala, which is involved in cortico-limbic circuits, has also been observed in...

  • Positive Facial Affect – An fMRI Study on the Involvement of Insula and Amygdala. Pohl, Anna; Anders, Silke; Schulte-Rüther, Martin; Mathiak, Klaus; Kircher, Tilo // PLoS ONE;Aug2013, Vol. 8 Issue 8, p1 

    Imitation of facial expressions engages the putative human mirror neuron system as well as the insula and the amygdala as part of the limbic system. The specific function of the latter two regions during emotional actions is still under debate. The current study investigated brain responses...

  • Facial Emotion Processing in Borderline Personality Disorder: A Systematic Review and Meta-Analysis. Mitchell, Amy; Dickens, Geoffrey; Picchioni, Marco // Neuropsychology Review;Jun2014, Vol. 24 Issue 2, p166 

    A body of work has developed over the last 20 years that explores facial emotion perception in Borderline Personality Disorder (BPD). We identified 25 behavioural and functional imaging studies that tested facial emotion processing differences between patients with BPD and healthy controls...

  • Down-regulation of amygdala activation with real-time fMRI neurofeedback in a healthy female sample. Paret, Christian; Kluetsch, Rosemarie; Ruf, Matthias; Demirakca, Traute; Hoesterey, Steffen; Ende, Gabriele; Schmahl, Christian // Frontiers in Behavioral Neuroscience;Sep2014, Vol. 8, p1 

    Psychiatric conditions of emotion dysregulation are often characterized by difficulties in regulating the activity of limbic regions such as the amygdala. Real-time functional magnetic resonance imaging (rt-fMRI) allows to feedback brain activation and opens the possibility to establish a...

  • Mindfulness and emotion regulation—an fMRI study. Lutz, Jacqueline; Herwig, Uwe; Opialla, Sarah; Hittmeyer, Anna; Jäncke, Lutz; Rufer, Michael; Grosse Holtforth, Martin; Brühl, Annette B. // Social Cognitive & Affective Neuroscience;Jun2014, Vol. 9 Issue 6, p776 

    Mindfulness—an attentive non-judgmental focus on present experiences—is increasingly incorporated in psychotherapeutic treatments as a skill fostering emotion regulation. Neurobiological mechanisms of actively induced emotion regulation are associated with prefrontally mediated...

  • Tension-related activity in the orbitofrontal cortex and amygdala: an fMRI study with music. Lehne, Moritz; Rohrmeier, Martin; Koelsch, Stefan // Social Cognitive & Affective Neuroscience;Oct2014, Vol. 9 Issue 10, p1515 

    Tonal music is characterized by a continuous flow of tension and resolution. This flow of tension and resolution is closely related to processes of expectancy and prediction and is a key mediator of music-evoked emotions. However, the neural correlates of subjectively experienced tension and...


Read the Article


Sorry, but this item is not currently available from your library.

Try another library?
Sign out of this library

Other Topics