Cited by 21Neuroendocrine regulation and behaviorStress Responses and CortisolNeurotransmitter Receptor Influence on Behavior

A single prolonged stress paradigm produces enduring impairments in social bonding in monogamous prairie voles

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Arai, Aki, Hirota, Yu, Miyase, Naoki, Miyata, Shiori, Young, Larry J., Osako, Yoji, Yuri, Kazunari, Mitsui, Shinichi·2016·Behavioural Brain Research

Abstract

Traumatic events such as natural disasters, violent crimes, tragic accidents, and war, can have devastating impacts on social relationships, including marital partnerships. We developed a single prolonged stress (SPS) paradigm, which consisted of restraint, forced swimming, and ether anesthesia, to establish an animal model relevant to post-traumatic stress disorder. We applied a SPS paradigm to a monogamous rodent, the prairie vole (Microtus ochrogaster) in order to determine whether a traumatic event affects the establishment of pair bonds. We did not detect effects of the SPS treatment on anhedonic or anxiety-like behavior. Sham-treated male voles huddled with their partner females, following a 6day cohabitation, for a longer duration than with a novel female, indicative of a pair bond. In contrast, SPS-treated voles indiscriminately huddled with the novel and partner females. Interestingly, the impairment of pair bonding was rescued by oral administration of paroxetine, a selective serotonin reuptake inhibitor (SSRI), after the SPS treatment. Immunohistochemical analyses revealed that oxytocin immunoreactivity (IR) was significantly decreased in the supraoptic nucleus (SON), but not in the paraventricular nucleus (PVN), 7days after SPS treatment, and recovered 14days after SPS treatment. After the presentation of a partner female, oxytocin neurons labeled with Fos IR was significantly increased in SPS-treated voles compared with sham-treated voles regardless of paroxetine administration. Our results suggest that traumatic events disturb the formation of pair bond possibly through an interaction with the serotonergic system, and that SSRIs are candidates for the treatment of social problems caused by traumatic events. Further, a vole SPS model may be useful for understanding mechanisms underlying the impairment of social bonding by traumatic events.

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Authors
Arai, A., Hirota, Y., Miyase, N., Miyata, S., Young, L. J., Osako, Y., Yuri, K., & Mitsui, S.
Affiliations
  • Gunma University (JP)
  • Emory University (US)
  • Kōchi University (JP)
Corresponding author
Mitsui, Shinichi
Venue
Behavioural Brain Research
Publisher
Elsevier BV
Published
2016-12
Volume
315
Pages
83-93
ISSN
0166-4328 (ISSN-L)
OpenAlex
W2513002667
Cited by
21
References
59
Citations by year
2026: 2 · 2025: 1 · 2024: 1 · 2023: 2 · 2021: 3 · 2020: 2 · 2019: 3 · 2018: 5 · 2017: 1 · 2016: 1
FWCI
5.23
Type
journal article
Language
en
Open access
Locations
  • Behavioural Brain Research (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • JSPS KAKENHI (26461734)
  • NIH (R01MH096983, 1P50MH100023, OD P51OD11132)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords
single prolonged stress, post-traumatic stress disorder, pair bonding, social bonding, Microtus ochrogaster, oxytocin, supraoptic nucleus, paraventricular nucleus, serotonergic system, paroxetine, selective serotonin reuptake inhibitors, traumatic stress, anhedonia, anxiety-like behavior, Fos expression
MeSH terms
Animals, Brain, Arvicolinae, Disease Models, Animal, Exploratory Behavior, Female, Male, Neurons, Oxytocin, Pair Bond, Receptors, Glucocorticoid, Stress Disorders, Post-Traumatic, Supraoptic Nucleus, Time Factors, Tyrosine 3-Monooxygenase, Selective Serotonin Reuptake Inhibitors, Paroxetine, Receptors, Vasopressin

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