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Prolonged partner separation erodes nucleus accumbens transcriptional signatures of pair bonding in male prairie voles

The loss of a spouse is often cited as the most traumatic event in a person’s life. However, for most people, the severity of grief and its maladaptive effects subside over time via an understudied adaptive process. Like humans, socially monogamous prairie voles (Microtus ochrogaster) form opposite-...

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Autores principales: Sadino, Julie M, Bradeen, Xander G, Kelly, Conor J, Brusman, Liza E, Walker, Deena M, Donaldson, Zoe R
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10112888/
https://www.ncbi.nlm.nih.gov/pubmed/36852906
http://dx.doi.org/10.7554/eLife.80517
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author Sadino, Julie M
Bradeen, Xander G
Kelly, Conor J
Brusman, Liza E
Walker, Deena M
Donaldson, Zoe R
author_facet Sadino, Julie M
Bradeen, Xander G
Kelly, Conor J
Brusman, Liza E
Walker, Deena M
Donaldson, Zoe R
author_sort Sadino, Julie M
collection PubMed
description The loss of a spouse is often cited as the most traumatic event in a person’s life. However, for most people, the severity of grief and its maladaptive effects subside over time via an understudied adaptive process. Like humans, socially monogamous prairie voles (Microtus ochrogaster) form opposite-sex pair bonds, and upon partner separation, show stress phenotypes that diminish over time. We test the hypothesis that extended partner separation diminishes pair bond-associated behaviors and causes pair bond transcriptional signatures to erode. Opposite-sex or same-sex paired males were cohoused for 2 weeks and then either remained paired or were separated for 48 hours or 4 weeks before collecting fresh nucleus accumbens tissue for RNAseq. In a separate cohort, we assessed partner-directed affiliation at these time points. We found that these behaviors persist despite prolonged separation in both same-sex and opposite-sex paired voles. Opposite-sex pair bonding led to changes in accumbal transcription that were stably maintained while animals remained paired but eroded following prolonged partner separation. Eroded genes are associated with gliogenesis and myelination, suggesting a previously undescribed role for glia in pair bonding and loss. Further, we pioneered neuron-specific translating ribosomal affinity purification in voles. Neuronally enriched transcriptional changes revealed dopaminergic-, mitochondrial-, and steroid hormone signaling-associated gene clusters sensitive to acute pair bond disruption and loss adaptation. Our results suggest that partner separation erodes transcriptomic signatures of pair bonding despite core behavioral features of the bond remaining intact, revealing potential molecular processes priming a vole to be able to form a new bond.
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spelling pubmed-101128882023-04-19 Prolonged partner separation erodes nucleus accumbens transcriptional signatures of pair bonding in male prairie voles Sadino, Julie M Bradeen, Xander G Kelly, Conor J Brusman, Liza E Walker, Deena M Donaldson, Zoe R eLife Neuroscience The loss of a spouse is often cited as the most traumatic event in a person’s life. However, for most people, the severity of grief and its maladaptive effects subside over time via an understudied adaptive process. Like humans, socially monogamous prairie voles (Microtus ochrogaster) form opposite-sex pair bonds, and upon partner separation, show stress phenotypes that diminish over time. We test the hypothesis that extended partner separation diminishes pair bond-associated behaviors and causes pair bond transcriptional signatures to erode. Opposite-sex or same-sex paired males were cohoused for 2 weeks and then either remained paired or were separated for 48 hours or 4 weeks before collecting fresh nucleus accumbens tissue for RNAseq. In a separate cohort, we assessed partner-directed affiliation at these time points. We found that these behaviors persist despite prolonged separation in both same-sex and opposite-sex paired voles. Opposite-sex pair bonding led to changes in accumbal transcription that were stably maintained while animals remained paired but eroded following prolonged partner separation. Eroded genes are associated with gliogenesis and myelination, suggesting a previously undescribed role for glia in pair bonding and loss. Further, we pioneered neuron-specific translating ribosomal affinity purification in voles. Neuronally enriched transcriptional changes revealed dopaminergic-, mitochondrial-, and steroid hormone signaling-associated gene clusters sensitive to acute pair bond disruption and loss adaptation. Our results suggest that partner separation erodes transcriptomic signatures of pair bonding despite core behavioral features of the bond remaining intact, revealing potential molecular processes priming a vole to be able to form a new bond. eLife Sciences Publications, Ltd 2023-02-28 /pmc/articles/PMC10112888/ /pubmed/36852906 http://dx.doi.org/10.7554/eLife.80517 Text en © 2023, Sadino et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Sadino, Julie M
Bradeen, Xander G
Kelly, Conor J
Brusman, Liza E
Walker, Deena M
Donaldson, Zoe R
Prolonged partner separation erodes nucleus accumbens transcriptional signatures of pair bonding in male prairie voles
title Prolonged partner separation erodes nucleus accumbens transcriptional signatures of pair bonding in male prairie voles
title_full Prolonged partner separation erodes nucleus accumbens transcriptional signatures of pair bonding in male prairie voles
title_fullStr Prolonged partner separation erodes nucleus accumbens transcriptional signatures of pair bonding in male prairie voles
title_full_unstemmed Prolonged partner separation erodes nucleus accumbens transcriptional signatures of pair bonding in male prairie voles
title_short Prolonged partner separation erodes nucleus accumbens transcriptional signatures of pair bonding in male prairie voles
title_sort prolonged partner separation erodes nucleus accumbens transcriptional signatures of pair bonding in male prairie voles
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10112888/
https://www.ncbi.nlm.nih.gov/pubmed/36852906
http://dx.doi.org/10.7554/eLife.80517
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