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

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...

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Autores principales: Bueno-Junior, Lezio S., Jones-Tinsley, Carolyn E., Milman, Noah E. P., Wickham, Peyton T., Watson, Brendon O., Lim, Miranda M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10336370/
https://www.ncbi.nlm.nih.gov/pubmed/37448475
http://dx.doi.org/10.1098/rsos.230700
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author Bueno-Junior, Lezio S.
Jones-Tinsley, Carolyn E.
Milman, Noah E. P.
Wickham, Peyton T.
Watson, Brendon O.
Lim, Miranda M.
author_facet Bueno-Junior, Lezio S.
Jones-Tinsley, Carolyn E.
Milman, Noah E. P.
Wickham, Peyton T.
Watson, Brendon O.
Lim, Miranda M.
author_sort Bueno-Junior, Lezio S.
collection PubMed
description 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.
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spelling pubmed-103363702023-07-13 Early-life sleep disruption impairs subtle social behaviours in prairie voles: a pose-estimation study Bueno-Junior, Lezio S. Jones-Tinsley, Carolyn E. Milman, Noah E. P. Wickham, Peyton T. Watson, Brendon O. Lim, Miranda M. R Soc Open Sci Organismal and Evolutionary Biology 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. The Royal Society 2023-07-12 /pmc/articles/PMC10336370/ /pubmed/37448475 http://dx.doi.org/10.1098/rsos.230700 Text en © 2023 The Authors. https://creativecommons.org/licenses/by/4.0/Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, provided the original author and source are credited.
spellingShingle Organismal and Evolutionary Biology
Bueno-Junior, Lezio S.
Jones-Tinsley, Carolyn E.
Milman, Noah E. P.
Wickham, Peyton T.
Watson, Brendon O.
Lim, Miranda M.
Early-life sleep disruption impairs subtle social behaviours in prairie voles: a pose-estimation study
title Early-life sleep disruption impairs subtle social behaviours in prairie voles: a pose-estimation study
title_full Early-life sleep disruption impairs subtle social behaviours in prairie voles: a pose-estimation study
title_fullStr Early-life sleep disruption impairs subtle social behaviours in prairie voles: a pose-estimation study
title_full_unstemmed Early-life sleep disruption impairs subtle social behaviours in prairie voles: a pose-estimation study
title_short Early-life sleep disruption impairs subtle social behaviours in prairie voles: a pose-estimation study
title_sort early-life sleep disruption impairs subtle social behaviours in prairie voles: a pose-estimation study
topic Organismal and Evolutionary Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10336370/
https://www.ncbi.nlm.nih.gov/pubmed/37448475
http://dx.doi.org/10.1098/rsos.230700
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