Mapping the vocal circuitry of Alston's singing mouse with pseudorabies virus.

Vocalizations are often elaborate, rhythmically structured behaviors. Vocal motor patterns require close coordination of neural circuits governing the muscles of the larynx, jaw, and respiratory system. In the elaborate vocalization of Alston's singing mouse (Scotinomys teguina) each note of its rapid, frequency-modulated trill is accompanied by equally rapid modulation of breath and gape. To elucidate the neural circuitry underlying this behavior, we introduced the polysynaptic retrograde neuronal tracer pseudorabies virus (PRV) into the cricothyroid and digastricus muscles, which control frequency modulation and jaw opening, respectively. Each virus singly labels ipsilateral motoneurons (nucleus ambiguus for cricothyroid, and motor trigeminal nucleus for digastricus). We find that the two isogenic viruses heavily and bilaterally colabel neurons in the gigantocellular reticular formation, a putative central pattern generator. The viruses also show strong colabeling in compartments of the midbrain including the ventrolateral periaqueductal gray and the parabrachial nucleus, two structures strongly implicated in vocalizations. In the forebrain, regions important to social cognition and energy balance both exhibit extensive colabeling. This includes the paraventricular and arcuate nuclei of the hypothalamus, the lateral hypothalamus, preoptic area, extended amygdala, central amygdala, and the bed nucleus of the stria terminalis. Finally, we find doubly labeled neurons in M1 motor cortex previously described as laryngeal, as well as in the prelimbic cortex, which indicate these cortical regions play a role in vocal production. The progress of both viruses is broadly consistent with vertebrate-general patterns of vocal circuitry, as well as with circuit models derived from primate literature.

Conservation and dimorphism in androgen receptor distribution in Alston's singing mouse (Scotinomys teguina).

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.

Social recognition is context dependent in single male prairie voles.

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.

Female alternative mating tactics, reproductive success and nonapeptide receptor expression in the social decision-making network.

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.

Oxytocin receptor density is associated with male mating tactics and social monogamy.

Despite its well-described role in female affiliation, the influence of oxytocin on male pairbonding is largely unknown. However, recent human studies indicate that this nonapeptide has a potent influence on male behaviors commonly associated with monogamy. Here we investigated the distribution of oxytocin receptors (OTR) throughout the forebrain of the socially monogamous male prairie vole (Microtus ochrogaster). Because males vary in both sexual and spatial fidelity, we explored the extent to which OTR predicted monogamous or non-monogamous patterns of space use, mating success and sexual fidelity in free-living males. We found that monogamous males expressed higher OTR density in the nucleus accumbens than non-monogamous males, a result that mirrors species differences in voles with different mating systems. OTR density in the posterior portion of the insula predicted mating success. Finally, OTR in the hippocampus and septohippocampal nucleus, which are nuclei associated with spatial memory, predicted patterns of space use and reproductive success within mating tactics. Our data highlight the importance of oxytocin receptor in neural structures associated with pairbonding and socio-spatial memory in male mating tactics. The role of memory in mating systems is often neglected, despite the fact that mating tactics impose an inherently spatial challenge for animals. Identifying mechanisms responsible for relating information about the social world with mechanisms mediating pairbonding and mating tactics is crucial to fully appreciate the suite of factors driving mating systems. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.

Beating the boojum: comparative approaches to the neurobiology of social behavior.

Neuropeptides coordinate complex social behaviors important to both basic and applied science. Understanding such phenomena requires supplementing the powerful tools of behavioral neuroscience with less conventional model species and more rigorous evolutionary analyses. We review studies that use comparative methods to examine the roles of vasopressin and oxytocin in mammalian social behavior. We find that oxytocin and vasopressin receptor distributions are remarkably variable within species. Studies of socially monogamous prairie voles reveal that pronounced individual differences in spatial memory structures (retrosplenial cortex and hippocampus) are better predictors of social and sexual fidelity than are areas known to regulate pairbonding directly, a pattern that seems to be mediated by the contributions of the neuropeptides to space use in natural settings. We next examine studies of individual and species differences in cis-regulatory regions of the avpr1a locus. While individual differences in social behaviors are linked to length of a microsatellite at the avpr1a locus, phylogenetic analyses reveal that the presence or absence of a microsatellite does not explain major differences between species. There seems to be no simple relationship between microsatellite length and behavior, but rather microsatellite length may be a marker for more subtle sequence differences between individuals. Lastly, we introduce the singing mouse, Scotinomys teguina, whose neuropeptide receptor distributions and unique natural history make it an exciting new model for mammalian vocalization and social cognition. The findings demonstrate how taxonomic and conceptual diversity provide a broader basis for understanding social behavior and its dysfunction.

Social investigation in a memory task relates to natural variation in septal expression of oxytocin receptor and vasopressin receptor 1a in prairie voles (Microtus ochrogaster).

Arginine vasopressin (AVP) and oxytocin (OT) influence social behavior and cognitive processes and may explain some of the variance associated with individual differences in behavior. Although great focus has been placed on the roles of these peptides in learning and memory, less attention has been given to the receptors to which they bind. The authors exposed male prairie voles (Microtus ochrogaster) to novel females in a multitrial social recognition test to investigate whether individual differences in vasopressin receptor (V1aR) or oxytocin receptor (OTR) related to social recognition. The authors also explored differences in OTR and V1aR throughout the brain to determine whether patterns of receptor coexpression emerged in functionally related structures. Male investigation of females was highly variable, and those that investigated females the most did not habituate to repeated female presentation. Moreover, high investigators expressed significantly more V1aR and less OTR in the lateral septum. Coexpression patterns of these receptors emphasize the role of OT and AVP in neural circuits involved in social behavior, reward, learning, and memory. Understanding individual differences in the laboratory may provide insight into evolved natural behavior.