Early-life sleep disruption impairs subtle social behaviours in prairie voles: a pose-estimation study

Author:

Bueno-Junior Lezio S.1ORCID,Jones-Tinsley Carolyn E.23ORCID,Milman Noah E. P.23ORCID,Wickham Peyton T.23ORCID,Watson Brendon O.1ORCID,Lim Miranda M.23ORCID

Affiliation:

1. Department of Psychiatry, University of Michigan Medical School, Ann Arbor, MI, USA

2. Veterans Affairs VISN20 Northwest MIRECC, VA Portland Health Care System, Portland, OR, USA

3. Oregon Alzheimer's Disease Research Center, Department of Neurology, Oregon Health and Science University, Portland, OR, USA

Abstract

Early-life sleep disruption (ELSD) has been shown to have long-lasting effects on social behaviour in adult prairie voles (Microtus ochrogaster), including impaired expression of pair bonding during partner preference testing. However, due to the limitations of manual behaviour tracking, the effects of ELSD across the time course of pair bonding have not yet been described, hindering our ability to trace mechanisms. Here, we used pose estimation to track prairie voles during opposite-sex cohabitation, the process leading to pair bonding. Male–female pairs were allowed to interact through a mesh divider in the home cage for 72 h, providing variables of body direction, distance-to-divider and locomotion speed. We found that control males displayed periodic patterns of body orientation towards females during cohabitation. In contrast, ELSD males showed reduced duration and ultradian periodicity of these body orientation behaviours towards females. Furthermore, in both sexes, ELSD altered spatial and temporal patterns of locomotion across the light/dark cycles of the 72 h recordings. This study allows a comprehensive behavioural assessment of the effects of ELSD on later life sociality and highlights subtle prairie vole behaviours. Our findings may shed light on neurodevelopmental disorders featuring sleep disruption and social deficits, such as autism spectrum disorders.

Funder

NSF NCS Foundations Award

Portland VA Research Foundation

National Institutes of Mental Health

Publisher

The Royal Society

Subject

Multidisciplinary

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