Brain functional connectivity modulates social bonding in monogamous voles

Abstract

Microtus ochrogaster, 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.

Inducing Partner Preference in Mice by Chemogenetic Stimulation of CA2 Hippocampal Subfield

“…Moreover, although evolutionary processes may lead to different neurochemical profiles in different brain regions (O'Connell and Hofmann, 2012) and epigenetic modifications may occur that are not attributable to changes in DNA sequence (Robinson et al, 2008), the social neural network's major nodes (McGraw and Young, 2010;Ko, 2017) are similar across the different species. Significant longitudinal changes following social bonding were described in the dorsal hippocampus of prairie voles (López-Gutiérrez et al, 2019). Also, within the social network, the CA2 subfield of the hippocampus is a key player in the modulation of social behaviors (Ko, 2017).…”

Role of Medial Prefrontal Cortical Neurons and Oxytocin Modulation in the Establishment of Social Buffering

“…The stress-induced release of corticosterone is reduced by social buffering, while the positive effects of the social buffering process can affect conditioning or extinction of fear memory, which is classified as a stress memory [ 4 - 6 ]. These social buffering-induced stress-relieving effects are mediated by various areas of the brain, such as the medial prefrontal cortex (mPFC), amygdala, bed nucleus of the stria terminalis, paraventricular nucleus, and nucleus accumbens [ 7 ]. The roles of the anterior cingulate cortex in empathy through the mirror neuron system, the prelimbic region (PL) in social recognition, and the infralimbic (IL) cortex in social memory suggest that the mPFC is related to social buffering associated with oxytocin [ 8 - 10 ].…”