Anxiogenic Potential of Experimental Sleep Fragmentation Is Duration-Dependent and Mediated via Oxidative Stress State

Author:

Grubač Željko1ORCID,Šutulović Nikola1ORCID,Šuvakov Sonja2ORCID,Jerotić Djurdja2ORCID,Puškaš Nela3ORCID,Macut Djuro4ORCID,Rašić-Marković Aleksandra1ORCID,Simić Tatjana2ORCID,Stanojlović Olivera1ORCID,Hrnčić Dragan1ORCID

Affiliation:

1. Institute of Medical Physiology “Richard Burian”, Belgrade University Faculty of Medicine, 11000 Belgrade, Serbia

2. Institute of Clinical and Medical Biochemistry, Belgrade University Faculty of Medicine, 11000 Belgrade, Serbia

3. Institute of Histology and Embryology “Aleksandar Đ. Kostić”, Belgrade University Faculty of Medicine, 11000 Belgrade, Serbia

4. Clinic of Endocrinology, Diabetes and Metabolic Disease, UCCS, Belgrade University Faculty of Medicine, 11000 Belgrade, Serbia

Abstract

Sleep architecture alterations, among which sleep fragmentation is highly prevalent, represent risk factors for a variety of diseases, ranging from cardiovascular to brain disorders, including anxiety. What mediates anxiety occurrence upon sleep fragmentation is still a matter of debate. We hypothesized that the sleep fragmentation effects on anxiety are dependent on its duration and mediated by increased oxidative stress and alterations in the number of parvalbumin (PV+) interneurons in the hippocampus. Sleep was fragmented in rats by the treadmill method during a period of 14 days (SF group). Rats with undisturbed sleep in the treadmill (TC group) and those receiving equal amounts of treadmill belt motion (EC group) served as controls. To assess anxiety, we subjected rats to the open field, elevated plus maze, and light-dark tests on the 0, 7th, and 14th day. Upon the last test, brain structures were sampled for oxidative stress assessment and PV+ interneuron immunohistochemistry. The results of ethological tests of anxiety-linked behavior suggested duration-dependent anxiogenic potential of sleep fragmentation. Rats’ anxiety-linked behavior upon sleep fragmentation significantly correlated with oxidative stress. The rats with fragmented sleep (SF) showed significantly higher oxidative stress in the hippocampus, thalamus, and cortex, compared to controls (TC and EC), while the antioxidant enzymes’ activity was significantly decreased. No significant differences were observed in hippocampal PV+ interneurons among these groups. Our results showed that duration of sleep fragmentation is a significant determinant of anxiety-linked behavior, and these effects are mediated through oxidative distress in the brain. Herein, it is revealed that the sleep fragmentation-oxidative stress-anxiety axis contributes to our better understanding of pathophysiological processes, occurring due to disrupted sleep patterns.

Funder

Ministarstvo Prosvete, Nauke i Tehnološkog Razvoja

Publisher

Hindawi Limited

Subject

Cell Biology,Ageing,General Medicine,Biochemistry

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