The prairie vole: an emerging model organism for understanding the social brain

Abstract

Unlike most mammalian species, the prairie vole is highly affiliative, forms enduring social bonds between mates and displays biparental behavior. Over two decades of research on this species has enhanced our understanding of the neurobiological basis not only of monogamy, social attachment and nurturing behaviors but also other aspects of social cognition. Because social cognitive deficits are hallmarks of many psychiatric disorders, discoveries made in prairie voles can direct novel treatment strategies for disorders such as autism spectrum disorder and schizophrenia. With the ongoing development of molecular, genetic and genomic tools for this species, prairie voles will likely maintain their current trajectory becoming an unprecedented model organism for basic and translational research focusing on the biology of the social brain.

Figure 1

The prairie vole as a model organism. A) This hamster-sized rodent forms selective social bonds with its partner and displays bi-parental behavior both in nature and in the laboratory (photograph provided by T. Ahern). There is considerable individual variation in social behavior, which is reflected by variation in neuropeptide receptor distributions in the brain. For example, the two autoradiograms on the left of B) illustrate the individual variation in OTR binding densities in the nucleus accumbens (NAcc) of female prairie voles, variation which has been linked to variation in alloparental behavior. Artificially increasing OTR binding using viral vector mediated gene transfer (right autoradiogram) facilitates partner preference formation in female (figure adapted from [16]). Thus, prairie voles are useful models for dissecting the neurobiological basis for diversity in behavior. C) Partner preference formation can be accurately quantified in a high-throughput manner using automated behavioral analysis systems (Figure adapted from [65]). D) Lentiviral transgenesis can now be used to manipulate the genome of prairie voles as demonstrated by the green prairie vole pups that are transgenic for expression of a green fluorescent protein (photograph provided by Z. Donaldson). This technique, when applied to behaviorally relevant genes, will facilitate research into understanding the relationship between genes and behavior. E) Genomic resources are rapidly becoming available for the prairie vole, including cytogenetic maps, single nucleotide polymorphism (SNP) panels, bacterial artificial chromosome (BAC) libraries, and the full genome is slated to be sequenced by NHGRI. Shown is fluorescent in situ hybridization (FISH) localizing two prairie vole BAC clones with known homology to the mouse genome to the prairie vole X chromosome.

Figure 2

A schematic illustrating the proposed neural circuitry of social bonding in prairie voles. Oxytocin (OT) neurons in the paraventricular nucleus of the hypothalamus (PVN) project to the nucleus accumbens (NAcc) as well as to the posterior pituitary [10]. Sociosexual interactions in female prairie voles stimulate the release of both OT and dopamine into the NAcc. In males, vasopressin neurons in the extended amygdala project to the ventral pallidum (VP) and the lateral septum (LS). Concurrently, olfactory signatures of the sexual partner are processed through the amygdala. It is hypothesized that the simultaneous activation of the neuropeptide and dopamine receptor systems in these regions leads to a conditioned partner preference by linking the rewarding nature of the sociosexual interaction and the olfactory signatures of the partner. Inter- and intra-species variation in OTR and AVPR1A in these regions contribute to diversity in social behaviors in voles. (Figure modified from [66].)