Social bonding induces changes in brain functional connectivity in male and female monogamous voles: a longitudinal fMRI study

, the prairie vole, has become a valuable rodent model to study complex social behaviors, including enduring social bonding. Previous studies have related pair bonding in the prairie vole with plastic changes in several brain regions. However, the network interaction between these regions and their relevance to such socio-sexual behaviors has yet to be described. In this study, we used resting state functional magnetic resonance imaging (rsfMRI) to explore the longitudinal changes in the functional interactions of a set of brain regions previously associated with pair bonding in prairie voles. Specifically, 32 prairie voles were scanned at baseline, after 24 hours and two weeks of cohabitation and mating with a sexual partner (16 male-female pairs). Between 48 and 72 hours of cohabitation voles showed significant preference for the partner over a stranger, confirming pair bond formation; however, individual variability was observed. Network based statistics showed no sex differences in functional connectivity, but revealed a common network with significant longitudinal changes between sessions, including the anterior cingulate cortex (ACC), anterior olfactory nucleus (AON), dentate gyrus (DG), dorsal hippocampus (dHIP), lateral septum (LS), medial prefrontal cortex (mPFC), retrosplenial cortex (RSC), ventral hippocampus (vHIP), and ventral tegmental area (VTA). Furthermore, baseline functional connectivity in three sub-networks including the ACC, nucleus accumbens (NAcc), basolateral amygdala, and DG (ACC-NAcc-BLA-DG), the medial amygdala (MeA)-ventral pallidum (VP), and RSC-VTA, predicted the onset of affiliative behavior (huddling latency) in the first hours of cohabitation, even before sexual experience. Finally, a relationship was found between the strength of the pair bond (partner preference index) with long-term changes in the functional connectivity between the ventral pallidum and medial amygdala (MeA-VP). Overall, our findings revealed the association between network-level changes and the process of social bonding, and provide a novel approach to further investigate the neurophysiology of complex social behaviors displayed in the prairie vole.