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Quiet wakefulness: The influence of intraperitoneal and intranasal oxytocin on sleep-wake behaviour and neurophysiology in rats

Joel S Raymond, Nicholas A Everett, Anand Gururajan, Michael T Bowen
doi: https://doi.org/10.1101/2022.11.23.514802
Joel S Raymond
1The University of Sydney, Faculty of Science, School of Psychology, Sydney, New South Wales, Australia
2The University of Sydney, Brain and Mind Centre, Sydney, New South Wales, Australia
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Nicholas A Everett
1The University of Sydney, Faculty of Science, School of Psychology, Sydney, New South Wales, Australia
2The University of Sydney, Brain and Mind Centre, Sydney, New South Wales, Australia
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Anand Gururajan
1The University of Sydney, Faculty of Science, School of Psychology, Sydney, New South Wales, Australia
2The University of Sydney, Brain and Mind Centre, Sydney, New South Wales, Australia
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Michael T Bowen
1The University of Sydney, Faculty of Science, School of Psychology, Sydney, New South Wales, Australia
2The University of Sydney, Brain and Mind Centre, Sydney, New South Wales, Australia
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  • For correspondence: michael.bowen@sydney.edu.au
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Abstract

Introduction Exogenous administration of the neuropeptide oxytocin exerts diverse effects on various neurobehavioural processes, including sleep and wakefulness. Since oxytocin can enhance attention to social and fear-related environmental cues, it should promote arousal and wakefulness. However, as oxytocin can attenuate stress, reduce activity, and elicit anxiolysis, oxytocin might also prime the brain for rest and promote sleep. At present, little research has comprehensively characterised the neuropsychopharmacology of oxytocin-induced effects on sleep-wake behaviour and no reconciliation of these two competing hypotheses has been proposed.

Methods This study explored the effects of oxytocin on sleep-wake outcomes using radiotelemetry-based polysomnography in adult male and female Wistar rats. Oxytocin was administered via intraperitoneal (i.p.; 0.1, 0.3 and 1 mg·kg-1) and intranasal (i.n.; 0.06, 1, 3 mg·kg-1) routes. Caffeine (i.p. and i.n.; 10 mg·kg-1) was administered as a wake-promoting positive control. To ascertain mechanism of action, pre-treatment experiments with the oxytocin receptor (OXTR) antagonist L-368,899 (i.p.; 5 mg·kg-1) followed by oxytocin (i.p.; 1 mg·kg-1) were also conducted.

Results In both male and female rats, i.p. oxytocin promoted quiet wakefulness at the cost of suppressing active wakefulness, NREM and REM sleep. Several i.p. oxytocin-induced sleep-wake effects were mediated by OXTR binding. In contrast, i.n. oxytocin did not alter most sleep-wake outcomes at any dose tested. Both i.p. and i.n. caffeine demonstrated wake-promoting effects.

Conclusions These findings help reconcile competing hypotheses of oxytocin-induced effects on sleep-wake behaviour: i.p. oxytocin promotes quiet wakefulness—a state of restful environmental awareness compatible with both oxytocin’s anxiolytic effects and its enhancement of processing complex stimuli.

Competing Interest Statement

MTB is an inventor on patents and patent applications covering oxytocin-based therapeutics. He is co-founder and Chief Scientific Officer of Kinoxis Therapeutics Pty Ltd, a company commercialising some of this intellectual property. The other author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted November 24, 2022.
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Quiet wakefulness: The influence of intraperitoneal and intranasal oxytocin on sleep-wake behaviour and neurophysiology in rats
Joel S Raymond, Nicholas A Everett, Anand Gururajan, Michael T Bowen
bioRxiv 2022.11.23.514802; doi: https://doi.org/10.1101/2022.11.23.514802
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Quiet wakefulness: The influence of intraperitoneal and intranasal oxytocin on sleep-wake behaviour and neurophysiology in rats
Joel S Raymond, Nicholas A Everett, Anand Gururajan, Michael T Bowen
bioRxiv 2022.11.23.514802; doi: https://doi.org/10.1101/2022.11.23.514802

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