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Partner Loss in Monogamous Rodents: Modulation of Pain and Emotional Behavior in Male Prairie Voles
Yoji Osako1, Reiko Nobuhara, Young-Chang P Arai
1From the Department of Neurobiology and Anatomy (Osako, Tanaka, Yuri), Kochi Medical School, Kochi University, Oko-cho, Nankoku, Kochi, Japan; Multidisciplinary Pain Centre, Aichi Medical University, School of Medicine (Nobuhara, Arai, Nishihara), Nagakute, Aichi, Japan; Center for Translational Social Neuroscience, Silvio O. Conte Center for Oxytocin and Social Cognition, Department of Psychiatry and Behavioral Sciences (Young), Yerkes National Primate Research Center, Emory University School of Medicine, Atlanta, GA; Center for Social Neural Networks, University of Tsukuba (Young), Tsukuba, Japan; and Department of Rehabilitation Sciences (Mitsui), Gunma University Graduate School of Health Sciences, Showa-machi, Maebashi, Gunma, Japan.
Objective:
Pain is modulated by psychosocial factors, and social stress-induced hyperalgesia is a common clinical symptom in pain disorders. To provide a new animal model for studying social modulation of pain, we examined pain behaviors in monogamous prairie voles experiencing partner loss.
Methods:
After cohabitation with novel females, males (n = 79) were divided into two groups on the basis of preference test scores. Half of the males of each group were separated from their partner (loss group), whereas the other half remained paired (paired group). Thus, males from both groups experienced social isolation. Open field tests, plantar tests, and formalin tests were then conducted on males to assess anxiety and pain-related behaviors.
Results:
Loss males showing partner preferences (n = 20) displayed a significant increase in anxiety-related behavior in the open-field test (central area/total distance: 13.65% [1.58%] for paired versus 6.45% [0.87%] for loss; p < .001), a low threshold of thermal stimulus in the plantar test (withdrawal latencies: 9.69 [0.98] seconds for paired versus 6.15 [0.75] seconds for loss; p = .037), and exacerbated pain behaviors in the formalin test (total number of lifts: 40.33 [4.46] for paired versus 54.42 [1.91] for loss; p = .042) as compared with paired males (n = 20). Thermal thresholds in the plantar test significantly correlated with anxiety-related behavior in the open-field test (r = 0.64). No such differences were observed in the males that did not display partner preferences (r = 0.15).
Conclusions:
Results indicate that social bonds and their disruption, but not social housing without bonding followed by isolation, modulate pain and emotion in male prairie voles. The prairie vole is a useful model for exploring the neural mechanisms by which social relationships contribute to pain and nociceptive processing in humans.