Neuropeptide S Counteracts Paradoxical Sleep Deprivation-Induced Anxiety-Like Behavior and Sleep Disturbances

Jun-Fan Xie; Yu-Feng Shao; Hai-Liang Wang; Can Wang; Guang-Fu Cui; Xiang-Pan Kong; Xiang-Pan Kong; Lin-Xin Wang; Yu-Nong Chen; Chao-Yu Cong; Hai-Lin Chen; Yi-Ping Hou

doi:10.3389/fncel.2018.00064

Frontiers in Cellular Neuroscience (Mar 2018)

Neuropeptide S Counteracts Paradoxical Sleep Deprivation-Induced Anxiety-Like Behavior and Sleep Disturbances

Jun-Fan Xie,
Yu-Feng Shao,
Hai-Liang Wang,
Can Wang,
Guang-Fu Cui,
Xiang-Pan Kong,
Xiang-Pan Kong,
Lin-Xin Wang,
Yu-Nong Chen,
Chao-Yu Cong,
Hai-Lin Chen,
Yi-Ping Hou

Affiliations

Jun-Fan Xie: Departments of Neuroscience, Anatomy, Histology, and Embryology, Key Laboratory of Preclinical Study for New Drugs of Gansu Province, School of Basic Medical Sciences, Lanzhou University, Lanzhou, China
Yu-Feng Shao: Departments of Neuroscience, Anatomy, Histology, and Embryology, Key Laboratory of Preclinical Study for New Drugs of Gansu Province, School of Basic Medical Sciences, Lanzhou University, Lanzhou, China
Hai-Liang Wang: Departments of Neuroscience, Anatomy, Histology, and Embryology, Key Laboratory of Preclinical Study for New Drugs of Gansu Province, School of Basic Medical Sciences, Lanzhou University, Lanzhou, China
Can Wang: Departments of Neuroscience, Anatomy, Histology, and Embryology, Key Laboratory of Preclinical Study for New Drugs of Gansu Province, School of Basic Medical Sciences, Lanzhou University, Lanzhou, China
Guang-Fu Cui: Departments of Neuroscience, Anatomy, Histology, and Embryology, Key Laboratory of Preclinical Study for New Drugs of Gansu Province, School of Basic Medical Sciences, Lanzhou University, Lanzhou, China
Xiang-Pan Kong: Departments of Neuroscience, Anatomy, Histology, and Embryology, Key Laboratory of Preclinical Study for New Drugs of Gansu Province, School of Basic Medical Sciences, Lanzhou University, Lanzhou, China
Xiang-Pan Kong: Department of Human Anatomy, School of Medicine, Hunan Normal University, Changsha, China
Lin-Xin Wang: Departments of Neuroscience, Anatomy, Histology, and Embryology, Key Laboratory of Preclinical Study for New Drugs of Gansu Province, School of Basic Medical Sciences, Lanzhou University, Lanzhou, China
Yu-Nong Chen: Departments of Neuroscience, Anatomy, Histology, and Embryology, Key Laboratory of Preclinical Study for New Drugs of Gansu Province, School of Basic Medical Sciences, Lanzhou University, Lanzhou, China
Chao-Yu Cong: Departments of Neuroscience, Anatomy, Histology, and Embryology, Key Laboratory of Preclinical Study for New Drugs of Gansu Province, School of Basic Medical Sciences, Lanzhou University, Lanzhou, China
Hai-Lin Chen: Departments of Neuroscience, Anatomy, Histology, and Embryology, Key Laboratory of Preclinical Study for New Drugs of Gansu Province, School of Basic Medical Sciences, Lanzhou University, Lanzhou, China
Yi-Ping Hou: Departments of Neuroscience, Anatomy, Histology, and Embryology, Key Laboratory of Preclinical Study for New Drugs of Gansu Province, School of Basic Medical Sciences, Lanzhou University, Lanzhou, China

DOI: https://doi.org/10.3389/fncel.2018.00064
Journal volume & issue: Vol. 12

Abstract

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Disturbed sleep is a common subjective complaint among individuals with anxiety disorders. Sleep deprivation increases general and specific anxiety symptoms among healthy individuals. The amygdala is critical for regulating anxiety and also involved in mediating the effects of emotions on sleep. Neuropeptide S (NPS) and NPS receptors (NPSR) are reported as a novel endogenous arousal and anxiolytic system, but it is unclear yet whether this system is involved in anxiety-like behavior and sleep caused by sleep deprivation, and how it plays anxiolytic effect underlying the comorbid condition. In the present study, we demonstrate that paradoxical sleep deprivation (PSD) induced by modified multiple platform method (MMPM) for 24 h caused anxiety-like behavior, a prolonged sleep latency and subsequent paradoxical sleep (PS) rebound accompanied by an increase in electroencephalogram (EEG) theta (4.5–8.5 Hz) activities across light and dark phase in rats. The increase of PS after PSD was due to an increase of episode number during light phase and both episode number and duration during dark phase. Central action of NPS (1 nmol) attenuated PSD-induced anxiety-like behavior, and altered PSD-induced sleep-wake disturbances through increasing wakefulness, and suppressing PS and EEG theta activities. The reduction in PS time following NPS administration during light phase was because of a decreased episode number. Furthermore, sleep amount in 24 h in PSD rats given NPS was lesser than that given saline. PSD significantly enhanced NPSR mRNA expression level in the amygdala. NPS remarkably increased the number of Fos-ir neurons in the basolateral amygdala (BLA), the central amygdala (CeA) and medial amygdala (MeA). The majority of Fos-ir neurons induced by NPS also expressed NPSR. These results suggest that NPSR upregulation in the amygdala is presumably related to the PSD-induced anxiety-like behavior and sleep disturbances, and that NPS counteracts PSD-induced anxiety-like behavior and sleep disturbances possibly through activating the neurons bearing NPSR in the amygdala. In addition, the little sleep increase in PSD rats treated with NPS suggests that NPS can function as an anxiolytic without causing a subsequent sleep rebound.

Published in Frontiers in Cellular Neuroscience

ISSN: 1662-5102 (Online)
Publisher: Frontiers Media S.A.
Country of publisher: Switzerland
LCC subjects: Medicine: Internal medicine: Neurosciences. Biological psychiatry. Neuropsychiatry
Website: http://www.frontiersin.org/cellular-neuroscience

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