The decision to mate may be one of the most important decisions that animals make. For monogamous species, this decision can carry the added weight of limiting future mating opportunities. The mechanisms that govern these decisions have presumably been shaped by evolution in ways that optimize decision-making processes. In particular, a so-called social decision-making network (SDM) has been proposed, which integrates brain structures comprising the ‘social behavior network’ with a neural system associated with reward. Here, we investigate the neural phenotypic differences in the SDM for oxytocin and vasopressin receptors (OTR, V1aR) of female socially monogamous prairie voles living in naturalistic conditions. We focus on these receptors because they are profoundly involved in mammalian social behavior. We found that V1aR in the bed nucleus of the stria terminalis, medial amygdala and ventral pallidum, and OTR in the nucleus accumbens and hippocampus significantly differed between pregnant and non-pregnant females. Most of these areas are more closely related to the reward component of the SDM. V1aR in the ventral pallidum was also greater in paired than in single females. Finally, reproductive success within mating tactics was related to receptor density in brain structures across the SDM, particularly those serving as the interface between the social behavior network and the reward system. Our data support the hypothesis that neural phenotype for neuromodulatory nonapeptide receptors within the SDM relates to natural behavior associated with reproductive decisions.
Single males might benefit from knowing the identity of neighbouring males when establishing and defending boundaries. Similarly, males should discriminate between individual females if this leads to more reproductive opportunities. Contextual social cues may alter the value of learning identity. Knowing the identity of competitors that intrude into an animal’s territory may be more salient than knowing the identity of individuals on whose territory an animal is trespassing. Hence, social and environmental context could affect social recognition in many ways. Here we test social recognition of socially monogamous single male prairie voles, Microtus ochrogaster. In experiment 1 we tested recognition of male or female conspecifics and found that males discriminated between different males but not between different females. In experiment 2 we asked whether recognition of males is influenced when males are tested in their own cage (familiar), in a clean cage (neutral) or in the home cage of another male (unfamiliar). Although focal males discriminated between male conspecifics in all three contexts, individual variation in recognition was lower when males were tested in their home cage (in the presence of familiar social cues) compared to when the context lacked social cues (neutral). Experiment 1 indicates that selective pressures may have operated to enhance male territorial behaviour and indiscriminate mate selection. Experiment 2 suggests that the presence of a conspecific cue heightens social recognition and that home-field advantages might extend to social cognition. Taken together, our results indicate social recognition depends on the social and possibly territorial context.
Early experiences can have enduring impacts on brain and behavior, but the strength of these effects can be influenced by genetic variation. In principle, polymorphic CpGs (polyCpGs) may contribute to gene-by-environment interactions (G × E) by altering DNA methylation. In this study, we investigate the influence of polyCpGs on the development of vasopressin receptor 1a abundance in the retrosplenial cortex (RSC-V1aR) of prairie voles (Microtus ochrogaster). Two alternative alleles ('HI'/'LO') predict RSC avpr1a expression, V1aR abundance and sexual fidelity in adulthood; these alleles differ in the frequency of CpG sites and in methylation at a putative intron enhancer. We hypothesized that the elevated CpG abundance in the LO allele would make homozygous LO/LO voles more sensitive to developmental perturbations. We found that genotype differences in RSC-V1aR abundance emerged early in ontogeny and were accompanied by differences in methylation of the putative enhancer. As predicted, postnatal treatment with an oxytocin receptor antagonist (OTA) reduced RSC-V1aR abundance in LO/LO adults but not their HI/HI siblings. Similarly, methylation inhibition by zebularine increased RSC-V1aR in LO/LO adults, but not in HI/HI siblings. These data show a gene-by-environment interaction in RSC-V1aR. Surprisingly, however, neither OTA nor zebularine altered adult methylation of the intronic enhancer, suggesting that differences in sensitivity could not be explained by CpG density at the enhancer alone. Methylated DNA immunoprecipiation-sequencing showed additional differentially methylated regions between HI/HI and LO/LO voles. Future research should examine the role of these regions and other regulatory elements in the ontogeny of RSC-V1aR and its developmentally induced changes.
Because of their roles in courtship and intrasexual competition, sexual displays are often sexually dimorphic, but we know little about the mechanisms that produce such dimorphism. Among mammals, one example is the vocalization of Alston's singing mouse (Scotinomys teguina), which consists of a series of rapidly repeated, frequency‐modulated notes. The rate and duration of songs is sexually dimorphic and androgen responsive. To understand the neuronal mechanisms underlying this sexual dimorphism, we map the sites of androgen sensitivity throughout the brain, focusing analysis along a pathway that spans from limbic structures to vocal motor regions. We find widespread expression of AR immunoreactivity (AR‐ir) throughout limbic structures important for social behavior and vocalization, including the lateral septum, extended amygdala, preoptic area and hypothalamus. We also find extensive AR staining along previously documented vocal motor pathways, including the periaqueductal gray, parabrachial nucleus, and nucleus ambiguus, the last of which innervates intrinsic laryngeal muscles. Lastly, AR‐ir is also evident in sensory areas such as the medial geniculate, inferior, and superior colliculi. A quantitative analysis revealed that males exhibited more AR‐ir than females, a pattern that was most pronounced in the hypothalamus. Despite the elaboration of vocalization in singing mice, comparison with prior literature suggests that the broad pattern of AR‐ir may be conserved across a wide range of rodents. Together these data identify brain nuclei well positioned to shape the sexually dimorphic vocalization of S. teguina and suggest that such androgen modulation of vocalization is evolutionary conserved among rodents.
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