Enhanced amygdala–cingulate connectivity associates with better mood in both healthy and depressive individuals after sleep deprivation

Author:

Chai Ya12ORCID,Gehrman Philip3ORCID,Yu Meichen45ORCID,Mao Tianxin12ORCID,Deng Yao12,Rao Joy2,Shi Hui26ORCID,Quan Peng27ORCID,Xu Jing12,Zhang Xiaocui28,Lei Hui29,Fang Zhuo210,Xu Sihua12,Boland Elaine311,Goldschmied Jennifer R.3,Barilla Holly3,Goel Namni12ORCID,Basner Mathias13ORCID,Thase Michael E.311,Sheline Yvette I.314,Dinges David F.13,Detre John A.2ORCID,Zhang Xiaochu11516ORCID,Rao Hengyi12ORCID

Affiliation:

1. Key Laboratory of Brain-Machine Intelligence for Information Behavior (Ministry of Education and Shanghai), School of Business and Management, Shanghai International Studies University, Shanghai 201620, China

2. Center for Functional Neuroimaging and Department of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104

3. Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104

4. Indiana Alzheimer’s Disease Research Center, School of Medicine, Indiana University, Indianapolis, IN 46202

5. Indiana University Network Science Institute, Bloomington, IN 47408

6. Beijing An Zhen Hospital, Capital Medical University, Beijing 100029, China

7. Research Center for Quality of Life and Applied Psychology, Guangdong Medical University, Dongguan, Guangdong 524023, China

8. Medical Psychological Center, The Second Xiangya Hospital, Central South University, Changsha, Hunan 410017, China

9. College of Education, Hunan Agricultural University, Changsha, Hunan 410127, China

10. Brain and Mind Research Institute, University of Ottawa, Ottawa, ON K1H 8M5, Canada

11. Mental Illness Research Education and Clinical Center, Corporal Michael J. Crescenz Veterans Affairs Medical Center, Philadelphia, PA 19104

12. Biological Rhythms Research Laboratory, Department of Psychiatry and Behavioral Sciences, Rush University Medical Center, Chicago, IL 60612

13. Division of Sleep and Chronobiology, Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104

14. Center for Neuromodulation in Depression and Stress, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104

15. Department of Radiology, the First Affiliated Hospital of University of Science and Technology of China, School of Life Science, Division of Life Science and Medicine, University of Science and Technology of China, Hefei, Anhui 230026, China

16. Department of Psychology, School of Humanities and Social Science, University of Science and Technology of China, Anhui 230026, China

Abstract

Sleep loss robustly disrupts mood and emotion regulation in healthy individuals but can have a transient antidepressant effect in a subset of patients with depression. The neural mechanisms underlying this paradoxical effect remain unclear. Previous studies suggest that the amygdala and dorsal nexus (DN) play key roles in depressive mood regulation. Here, we used functional MRI to examine associations between amygdala- and DN-related resting-state connectivity alterations and mood changes after one night of total sleep deprivation (TSD) in both healthy adults and patients with major depressive disorder using strictly controlled in-laboratory studies. Behavioral data showed that TSD increased negative mood in healthy participants but reduced depressive symptoms in 43% of patients. Imaging data showed that TSD enhanced both amygdala- and DN-related connectivity in healthy participants. Moreover, enhanced amygdala connectivity to the anterior cingulate cortex (ACC) after TSD associated with better mood in healthy participants and antidepressant effects in depressed patients. These findings support the key role of the amygdala–cingulate circuit in mood regulation in both healthy and depressed populations and suggest that rapid antidepressant treatment may target the enhancement of amygdala–ACC connectivity.

Funder

HHS | NIH | National Heart, Lung, and Blood Institute

HHS | NIH | National Institute of Mental Health

HHS | NIH | National Institute on Aging

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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