Abstract:Here we discuss the origins of diversity in social behavior by highlighting research using the socially monogamous prairie vole. Prairie voles display a rich social behavioral repertoire involving pair bonding and consoling behavior that are not observed in typical laboratory species. Oxytocin and vasopressin play critical roles in regulating pair bonding and consoling behavior. Oxytocin and vasopressin receptors show remarkable diversity in expression patterns both between and within species. Receptor express… Show more
“…It is noteworthy that the highly variable distributions of forebrain vasopressin receptors across species stands in stark contrast to the deeply conserved patterning of other neuromodulatory systems such as steroid hormone and dopamine receptors (King & Young, 2016). This evidence in conjunction with our data lends credence to the notion that VP systems exhibit high levels of evolvability that may enable this hormonal signal to take on new functions in the modulation of social behavior (Young & Zhang, 2021).…”
The impact of variation in parental caregiving has lasting implications for the development of offspring. However, the ways in which parents impact each other in the context of caregiving is comparatively less understood, but can account for much of the variation observed in the postnatal environment. Prairie voles (Microtus ochrogaster) demonstrate a range of postnatal social groups, including biparental pairs and pups raised by their mothers alone. In addition to the challenges of providing parental care, prairie vole parents often experience acute natural stressors (e.g., predation, foraging demands, thermoregulation) that could alter the way co-parents interact. We investigated how variation in the experience of raising offspring impacts parental behavior and neurobiology by administering an acute handling stressor on prairie vole families of single mothers and biparental parents over the course of offspring postnatal development. Mothers and fathers exhibited robust behavioral plasticity in response to the age of their pups, but in sex-dependent ways. Pup-directed care from mothers did not vary as a function of their partner’s presence, but did covary with the number of hypothalamic vasopressin neurons in experience-dependent ways. The relationship between vasopressin neuron numbers and fathers’ behaviors was also contingent upon the stress handling manipulation, suggesting that brain-behavior associations exhibit stress-induced plasticity. These results demonstrate that the behavioral and neuroendocrine profiles of adults are sensitive to distinct and interacting experiences as a parent, and extend our knowledge of the neural mechanisms that may facilitate parental behavioral plasticity.
“…It is noteworthy that the highly variable distributions of forebrain vasopressin receptors across species stands in stark contrast to the deeply conserved patterning of other neuromodulatory systems such as steroid hormone and dopamine receptors (King & Young, 2016). This evidence in conjunction with our data lends credence to the notion that VP systems exhibit high levels of evolvability that may enable this hormonal signal to take on new functions in the modulation of social behavior (Young & Zhang, 2021).…”
The impact of variation in parental caregiving has lasting implications for the development of offspring. However, the ways in which parents impact each other in the context of caregiving is comparatively less understood, but can account for much of the variation observed in the postnatal environment. Prairie voles (Microtus ochrogaster) demonstrate a range of postnatal social groups, including biparental pairs and pups raised by their mothers alone. In addition to the challenges of providing parental care, prairie vole parents often experience acute natural stressors (e.g., predation, foraging demands, thermoregulation) that could alter the way co-parents interact. We investigated how variation in the experience of raising offspring impacts parental behavior and neurobiology by administering an acute handling stressor on prairie vole families of single mothers and biparental parents over the course of offspring postnatal development. Mothers and fathers exhibited robust behavioral plasticity in response to the age of their pups, but in sex-dependent ways. Pup-directed care from mothers did not vary as a function of their partner’s presence, but did covary with the number of hypothalamic vasopressin neurons in experience-dependent ways. The relationship between vasopressin neuron numbers and fathers’ behaviors was also contingent upon the stress handling manipulation, suggesting that brain-behavior associations exhibit stress-induced plasticity. These results demonstrate that the behavioral and neuroendocrine profiles of adults are sensitive to distinct and interacting experiences as a parent, and extend our knowledge of the neural mechanisms that may facilitate parental behavioral plasticity.
“…Interestingly, while prairie voles have high densities of OXTR binding in the basolateral amygdala, mice do not (L. J. Young & Zhang, 2021). Strong Oxtr labeling was also detected in the anterior olfactory area and granule cell layer of the olfactory bulb.…”
Section: Discussionmentioning
confidence: 99%
“…It is important to note that OXTR-binding patterns have been shown to vary widely between rodent species (Raggenbass et al, 1989; L. J. Young & Zhang, 2021).…”
Section: Mismatches In the Localization Of Oxtr Mrna And Oxtr Proteinmentioning
Oxytocin regulates social behavior via direct modulation of neurons, regulation of neural network activity, and interaction with other neurotransmitter systems. The behavioral effects of oxytocin signaling are determined by the species‐specific distribution of brain oxytocin receptors. The socially monogamous prairie vole has been a useful model organism for elucidating the role of oxytocin in social behaviors, including pair bonding, response to social loss, and consoling. However, there has been no comprehensive mapping of oxytocin receptor‐expressing cells throughout the prairie vole brain. Here, we employed a highly sensitive in situ hybridization, RNAscope, to construct an exhaustive, brain‐wide map of oxytocin receptor mRNA‐expressing cells. We found that oxytocin receptor mRNA expression was widespread and diffused throughout the brain, with specific areas displaying a particularly robust expression. Comparing receptor binding with mRNA revealed that regions of the hippocampus and substantia nigra contained oxytocin receptor protein but lacked mRNA, indicating that oxytocin receptors can be transported to distal neuronal processes, consistent with presynaptic oxytocin receptor functions. In the nucleus accumbens, a region involved in oxytocin‐dependent social bonding, oxytocin receptor mRNA expression was detected in both the D1 and D2 dopamine receptor‐expressing subtypes of cells. Furthermore, natural genetic polymorphisms robustly influenced oxytocin receptor expression in both D1 and D2 receptor cell types in the nucleus accumbens. Collectively, our findings further elucidate the extent to which oxytocin signaling is capable of influencing brain‐wide neural activity, responses to social stimuli, and social behavior.
Key points
Oxytocin receptor mRNA is diffusely expressed throughout the brain, with strong expression concentrated in certain areas involved in social behavior.
Oxytocin receptor mRNA expression and protein localization are misaligned in some areas, indicating that the receptor protein may be transported to distal processes.
In the nucleus accumbens, oxytocin receptors are expressed on cells expressing both D1 and D2 dopamine receptor subtypes, and the majority of variation in oxytocin receptor expression between animals is attributable to polymorphisms in the oxytocin receptor gene.
“…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. investigation, mating, allogrooming, etc), and it may be that the structure/function differences in the NAc oxytocin system are what evolution has shaped to enable the same social neuropeptide to facilitate distinct, species-specific pro-social behaviours [37,38]. Figure 1Representative autoradiograms showing distinct patterns of OXTR binding in the NAc of mouse (left) and prairie vole (right).…”
Section: Diverse Sources Of Variation In the Nucleus Accumbens Oxytoc...mentioning
Oxytocin modulates social behaviour across diverse vertebrate taxa, but the precise nature of its effects varies across species, individuals and lifetimes. Contributing to this variation is the fact that oxytocin's physiological effects are mediated through interaction with diverse neuromodulatory systems and can depend on the specifics of the local circuits it acts on. Furthermore, those effects can be influenced by both genetics and experience. Here we discuss this complexity through the lens of a specific neuromodulatory system, endocannabinoids, interacting with oxytocin in the nucleus accumbens to modulate prosocial behaviours in prairie voles. We provide a survey of current knowledge of oxytocin–endocannabinoid interactions in relation to social behaviour. We review in detail recent research in monogamous female prairie voles demonstrating that social experience, such as mating and pair bonding, can change how oxytocin modulates nucleus accumbens glutamatergic signalling through the recruitment of endocannabinoids to modulate prosocial behaviour toward the partner. We then discuss potential sex differences in experience-dependent modulation of the nucleus accumbens by oxytocin in voles based on new data in males. Finally, we propose that future oxytocin-based precision medicine therapies should consider how prior social experience interacts with sex and genetics to influence oxytocin actions.
This article is part of the theme issue ‘Interplays between oxytocin and other neuromodulators in shaping complex social behaviours’.
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