Indispensable role of the oxytocin receptor for allogrooming toward socially distressed cage mates in female mice

Abstract

Social contact reduces stress responses in social animals. Mice have been shown to show allogrooming behaviour toward distressed conspecifics. However, the precise neuronal mechanisms underlying allogrooming behaviour remain unclear. In the present study, we examined whether mice show allogrooming behaviour towards distressed conspecifics in a social defeat model and we also determined whether oxytocin receptor‐expressing neurons were activated during allogrooming by examining the expression of c‐Fos protein, a marker of neurone activation. Mice showed allogrooming behaviour toward socially defeated conspecifics. After allogrooming behaviour, the percentages of oxytocin receptor‐expressing neurones expressing c‐Fos protein were significantly increased in the anterior olfactory nucleus, cingulate cortex, insular cortex, lateral septum and medial amygdala of female mice, suggesting that oxytocin receptor‐expressing neurones in these areas were activated during allogrooming behaviour toward distressed conspecifics. The duration of allogrooming was correlated with the percentages of oxytocin receptor‐expressing neurones expressing c‐Fos protein in the anterior olfactory nucleus, insular cortex, lateral septum and medial amygdala. In oxytocin receptor‐deficient mice, allogrooming behaviour toward socially defeated cage mates was markedly reduced in female mice but not in male mice, indicating the importance of the oxytocin receptor for allogrooming behaviour in female mice toward distressed conspecifics. The results suggest that the oxytocin receptor, possibly in the anterior olfactory nucleus, insular cortex, lateral septum and/or medial amygdala, facilitates allogrooming behaviour toward socially distressed familiar conspecifics in female mice.

Hearing, touching, and multisensory integration during mate choice

“…Intriguingly insula function may be decisive to discriminate between sick and healthy rats (Rieger et al, 2022 ) whereas the amygdala seems to have a preventive but not a causal role (Kwon et al, 2021 ) in signaling sickness and overall sociability. Affective touch during social encounters has been shown to modulate insula activity in rats (Rogers-Carter et al, 2018 ; Miura et al, 2020 ) and mice (Miura et al, 2020 ; Matsumoto et al, 2021 ) while there are no studies evaluating insular modulation by social vocalizations or USV in general. Even though multimodal processing in the insula has been described in the rat and mouse (Rodgers et al, 2008 ; Gogolla et al, 2014 ) and causal insular impact during social cognition (Rogers-Carter et al, 2018 ; Rogers-Carter and Christianson, 2019 ), such as novelty recognition (Kim et al, 2021 ) has been demonstrated, mate choice studies measuring insula activity during the different phases are missing.…”

Roles of Oxytocin in Stress Responses, Allostasis and Resilience

“…Allogrooming decreases anxiety-related behaviors and corticosterone levels [ 86 ]. Mandarin voles [ 87 ] and female mice [ 88 ] have also been reported to show consolation-like allogrooming behavior towards socially defeated partners via the oxytocin system.…”

Emotional contagion and prosocial behavior in rodents

“…This is similar to how stimulus enhancement, the fact that animals will pay more attention to objects manipulated by others, is not true imitation but can still facilitate it [131]. Interestingly, proximity seeking and allogrooming are triggered by brain structures also involved in emotional contagion, including the central [109] and medial amygdala [117,119], area 24 [115,117,120,121,128], and insular cortex [113,117,132], and this activity is often modulated by the oxytocin system [115,117,120]. The social transmission of stress and the buffering effect that result from these behaviors have been shown to increase and decrease, respectively, the hypothalamic and hippocampal plasticity normally associated with stress [116,118,124].…”

“…(Figure 4B), in which an observer can freely interact with a demonstrator that has been stressed (e.g., previously restrained, defeated, shocked, acid or bee venom injected, or presented with a CS+), the observer not only approaches but also sniffs, licks, touches, and allogrooms the stressed demonstrator and does so more often and for longer than when interacting with a nonstressed conspecific [27,49,66,[114][115][116][117][118][119]. The stressed demonstrator, in contrast, engages more in nonsocial behaviors such as self-grooming, digging, rearing, and nesting [115,118,119].…”

“…Proximity seeking can thus also be conceived of as a form of consolation that benefits the approached demonstrator [5,12,49,66,[114][115][116]120,121,128]. Given such benefits for the observer and the demonstrator, it is perhaps not surprising that this propensity to approach and the increased allogrooming, licking, and sniffing are so ubiquitous in rats, mice, and voles and have been documented in males and females [66,114,115,119,120], although more strongly towards familiar conspecifics [27,49,66,[114][115][116][117]. However, the information benefits for the observer raise the question of whether the primary motivation for observers is to console or to seek information.…”