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

• Authors: Aki Arai, Gunma University; Yu Hirota, Gunma University; Naoki Miyase, Gunma University; Shiori Miyata, Gunma University; Larry Young, Emory University; Yoji Osako, Kochi University; Kazunari Yuri, Kochi University; Shinichi Mitsui, Gunma University
• Journal Title: Behavioural Brain Research
• Volume: Volume 315
• Publisher: Elsevier | 2016-12-15, Pages 83-93
• Type of Work: Article | Post-print: After Peer Review
• Publisher DOI: http://doi.org/10.1016/j.bbr.2016.08.022
• Subjects: Psychology, Social; Biology, Animal Physiology
• Keywords: Science & Technology; Life Sciences & Biomedicine; Behavioral Sciences; Neurosciences; Neurosciences & Neurology; PTSD; Partner preference; Social behavior; Serotonin; SSRI; Paroxetine; POSTTRAUMATIC-STRESS; MICROTUS-OCHROGASTER; PARTNER PREFERENCE; MESSENGER-RNA; FAST FEEDBACK; RAT MODEL; OXYTOCIN; VASOPRESSIN; EXPRESSION; DISORDER

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 6 day 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), 7 days after SPS treatment, and recovered 14 days 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.