Transcriptomic Regulations Underlying Pair-bond Formation and Maintenance in the Socially Monogamous Male and Female Prairie Vole

Duclot, Florian; Sailer, Lindsay L.; Koutakis, Panagiotis; Wang, Zuoxin; Kabbaj, Mohamed

doi:10.1016/j.biopsych.2020.11.022

Cited by 17 publications

(24 citation statements)

References 60 publications

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“…Together, these terms implicate processes central to neuronal remodeling and synaptic plasticity. Of note, while our analyses do identify a number of mitochondrial GO terms, these terms are not as strongly implicated in our analyses as in previous reports ( 20 ). However, mitochondrial terms are still represented and, together, our studies support that mitochondrial dynamics in the NAc are likely important for male prairie vole pair bonding.…”

Section: Discussioncontrasting

confidence: 74%

“…Changes in many behavioral states, such as a shift in dominance or reproductive status, are supported by stable changes in transcription, although this has not been examined in the context of pair bonds (30)(31)(32). While prior work has demonstrated that mating and cohabitation in prairie voles result in transcriptional changes within the NAc, the consistency of these changes as long as the bond remains intact has yet to be assessed (33)(34)(35)(36)(37). Thus, we compared NAc transcription in opposite-versus same-sexpaired voles following either 2 or 6 weeks of pairing/cohabitation (Fig.…”

Section: The Pair Bond Transcriptional Signature Is Stable Over Timementioning

confidence: 99%

“…Comparison of opposite-sex and same-sex prairie vole pairs provides a powerful means to identify the neurobiological changes specific to pair bonding independent of those that support affiliative relationships more generally (4,(17)(18)(19). Specifically, pair bonds, when compared to same-sex pairs, induce altered neuropeptide signaling and receptor expression throughout the brain (10,(20)(21)(22)(23)(24). In both sexes, formation of a pair bond yields a robust change in transcription in the nucleus accumbens (NAc), a brain region extensively implicated in pair bonding and loss adaptation (20,21).…”

Section: Introductionmentioning

confidence: 99%

“…Specifically, pair bonds, when compared to same-sex pairs, induce altered neuropeptide signaling and receptor expression throughout the brain (10,(20)(21)(22)(23)(24). In both sexes, formation of a pair bond yields a robust change in transcription in the nucleus accumbens (NAc), a brain region extensively implicated in pair bonding and loss adaptation (20,21). Such pair bondinduced transcriptional changes may solidify the exclusive rewarding aspects of a bond, and by this logic, it is likely that transcriptional changes in the NAc are also important for adapting to partner loss.…”

Section: Introductionmentioning

confidence: 99%

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

Sadino

Bradeen

Kelly

et al. 2021

Preprint

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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 behavioral and neuroendocrine stress phenotypes that diminish over time. Eventually, they can form a new bond, a key indicator of adapting to the loss of their partner. Thus, prairie voles provide an ethologically-relevant model for examining neuromolecular changes that emerge following partner separation for adapting to loss. Here, we test the hypothesis that extended partner separation diminishes pair bond-associated behaviors (partner preference and selective aggression) and causes pair bond transcriptional signatures to erode. Pairs were cohoused for 2 weeks and then either remained paired or were separated for 48hrs or 4wks before collecting fresh nucleus accumbens tissue for RNAseq. In a separate cohort, we assessed partner preference and selective aggression at these time points. Surprisingly, pair bond-associated behaviors persist despite prolonged separation and are similar between same-sex and opposite-sex paired voles. In contrast, we found that opposite-sex pair bonding, as compared with same-sex pairing, led to changes in accumbal transcription that were stably maintained as long as animals remained paired but eroded following prolonged partner separation. Eroded genes are primarily associated with gliogenesis and myelination, suggesting a previously undescribed role for glia in maintaining pair bonds and adapting to partner loss. We further reasoned that relevant neuronal transcriptional changes may have been masked by the prominent transcriptional signals associated with glia. Thus, we pioneered neuron-specific translating ribosomal affinity purification in voles. Neuronally-enriched transcriptional changes revealed dopaminergic-, mitochondrial-, and steroid hormone signaling-associated gene clusters whose expression patterns are sensitive to acute pair bond disruption and loss adaptation. Together, our results suggest that partner separation results in erosion of transcriptomic signatures of pair bonding despite core behavioral features of the bond remaining intact, revealing potential molecular processes central to priming a vole to be able to form a new bond.

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Section: Discussioncontrasting

confidence: 74%

Section: The Pair Bond Transcriptional Signature Is Stable Over Timementioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

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

Sadino

Bradeen

Kelly

et al. 2021

Preprint

View full text Add to dashboard Cite

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“…In fact, we know surprisingly little about the mechanisms and consequences underlying individual differences in social bonding across species. We also currently have a poor understanding of how social bonds change over time 27–31 or how such dynamic relationships produce enduring impacts on individuals' brain and behavior 32,33 . Such gaps in our understanding have implications for both basic and applied research.…”

Section: Introductionmentioning

confidence: 99%

Reciprocal processes of sensory perception and social bonding: an integrated social‐sensory framework of social behavior

Prior

Bentz

Ophir

2021

Genes Brain and Behavior

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Organisms filter the complexity of natural stimuli through their individual sensory and perceptual systems. Such perceptual filtering is particularly important for social stimuli.A shared "social umwelt" allows individuals to respond appropriately to the expected diversity of cues and signals during social interactions. In this way, the behavioral and neurobiological mechanisms of sociality and social bonding cannot be disentangled from perceptual mechanisms and sensory processing. While a degree of embeddedness

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A Neuroscientist's Guide to the Vole

2021

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Prairie voles have emerged as an important rodent model for understanding the neuroscience of social behavior. Prairie voles are well known for their capacity for pair bonding and alloparental care. These behavioral phenomena overlap with human social behavior but are not commonly observed in traditional rodent models. In this article, we highlight the many benefits of using prairie voles in neuroscience research. We begin by describing the advantages of using diverse and non‐traditional study models. We then focus on social behaviors, including pair bonding, alloparental care, and peer interactions, that have brought voles to the forefront of social neuroscience. We describe many additional features of prairie vole biology and behavior that provide researchers with opportunities to address an array of research questions. We also survey neuroethological methods that have been used with prairie voles, from classic to modern techniques. Finally, we conclude with a discussion of other vole species, particularly meadow voles, and their own unique advantages for neuroscience studies. This article provides a foundation for researchers who are new to working with voles, as well as for experienced neuroscientists who want to expand their research scope. © 2021 Wiley Periodicals LLC.

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Transcriptomic Regulations Underlying Pair-bond Formation and Maintenance in the Socially Monogamous Male and Female Prairie Vole

Cited by 17 publications

References 60 publications

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

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

Reciprocal processes of sensory perception and social bonding: an integrated social‐sensory framework of social behavior

A Neuroscientist's Guide to the Vole

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