Social Experience Alters Oxytocinergic Modulation in the Nucleus Accumbens of Female Prairie Voles

Sex-specific and social experience-dependent oxytocin–endocannabinoid interactions in the nucleus accumbens: implications for social behaviour

“…And while mating in female prairie voles during pair bond formation reportedly increases oxytocin and vasopressin receptor levels in the NAc [56], that alone could not explain why a female might behave affiliatively toward its partner but aggressively towards a stranger. Instead, the physiological actions of oxytocin in different contexts—defined by both external factors and internal biological conditions—need to be carefully examined, with particular attention to the wide diversity of other neuromodulators such as dopamine [57], serotonin [33], vasopressin [58] or eCBs [34,59] with which oxytocin interacts. Among these, we focus here on eCBs, which play an important role in reward and reinforcement during social experience-dependent plasticity.…”

“…Since social experience changes how oxytocin works through eCBs in the female prairie vole NAc, we wondered whether the same occurs in male prairie voles after cohabitation, or whether sex serves in this case as another source of variation in oxytocin's physiological actions. Thus, as a final illustration of oxytocin's complex neuromodulatory mechanisms, we evaluated whether the identical social experience protocol used to demonstrate a TGOT-induced experience-dependent potentiation in females [34] would produce the same result in males. We performed in vitro field potential recordings in paired males after a 24 h cohabitation with a sexually receptive female, and applied TGOT in the bath while electrically stimulating to induce excitatory responses in the NAc.…”

“…Thus, mouse and vole display markedly different distributions of oxytocin receptors in the NAc leading to different physiological effects (figure 1) [36]. In mice, OXTR activation and interaction with serotonin results in synaptic depression in NAc [33], whereas OXTR activation in pair-bonded female prairie voles produces a potentiation of glutamatergic neurotransmission in the NAc [34]. Of course, these two species have divergent socio-sexual behavioural repertoires (bi-parental rearing of pups and social monogamy in voles but not mice) on top of common rodent social behaviours (e.g.…”

“…Finally, the fact that eCBs mediate the pair-bonded female's oxytocin-potentiated excitatory signals in the NAc may indicate that it is the rewarding aspects of partner-specific social interactions that are being transmitted to bias the active selection of an affiliative behavioural response. This may explain why blocking CB1 receptors in vivo in pair-bonded female voles selectively prevents their normal tendency to reduce how long they spend aggressively rejecting their partner in an upright posture, compared to their rejection of a stranger [34], even though it does not strongly affect the duration of passive huddling with their partner [91].…”

“…Thus, if oxytocin–eCB interactions do facilitate selective social reward, then this coupling might be expected to change after positive social experience leading to a pair bond, such as mating. We recently investigated this possibility in female prairie voles [34]. We showed that an interaction between oxytocin and eCBs indeed emerges in an experience-dependent way.…”