Transgenerational Differences between Two Culturally Distinct Prairie Vole Populations

Culture can be described as a system of environmental beliefs, values, and social practices within one’s environment. This system is passed on from generation to generation and provides a basis for an individual’s behaviors and cognitive perceptions. Cultural neuroscience is an emerging field that intertwines domains of anthropology, psychology, neuroscience, and genetics to help understand the underlying processes, neural mechanisms and genomic factors that vary across cultures. Similar to humans, the socially monogamous prairie vole (Microtus ochrogaster) display populational differences in prosocial behavior and aggression based upon region-specific cultural upbringing and parental lineage. Prairie voles originating from Kansas (KS) display significantly lower levels of prosocial behavior and higher levels of aggression than voles from Illinois (IL). Behavioral differences are associated with significant differences in the underlying mechanisms, including expression of central estrogen receptor alpha (ERα), oxytocin, and vasopressin. Male hybrid offspring from both populations follow the maternal population’s behavioral pattern, with KI male offspring (KS dam and IL sire) displaying a significant overexpression of ERα in a number of important regions of the brain that regulate prosocial behavior. A major goal of this study was to take advantage of these exaggerated phenotypes to determine if there are also differences associated with population of origin within the neural networks that regulate social behavior using functional magnetic resonance imaging (fMRI). First, we examined if there were differences in microarchitecture and functional resting-state connectivity between KI and IL males. We found that there were significant differences in gray matter microarchitecture and functional connectivity among KI and IL males. IL males had significantly higher gray matter microarchitecture and functional connectivity in regions relevant to prosocial behavior, including the bed nucleus of the stria terminalis (BST), paraventricular nucleus of the hypothalamus, and the anterior thalamic nuclei. Our results support the hypothesis that gray matter microarchitecture and functional connectivity are associated with the expression of prosocial behavior. Second, by using graph theory network analysis on the aforementioned fMRI data, we identified a presumptive “prosocial” core (PS core) of nodes based on regions empirically studied to contribute to the prosocial behavior, in addition to an olfactory core (O core). Our goal was to elucidate the fundamental network connectivity globally (total connections), locally (within-core connections), and between nodes associated with the prosocial and olfactory core. Our results found that the global connectivity of the O core is similar in both males, while IL males displayed a higher degree of connectivity globally, within the PS core, and between the O and PS cores. Lastly, we examined a sample of the genomes for IL, KS, KI, and IK (IL dam x KS sire) groups. We used double digest restriction-site associated DNA (ddRADseq) to examine 7,813 autosomal ddRADseq loci, 202 X-chromosome loci, and 11 Y-chromosome loci. We found that among all groups, there was overall genetic similarity, with only a few outlier regions. Of these putative outliers, we found significant differences among populations (KS vs. IL), as well as parent-hybrid differences (IL vs. IK, IL vs. KI). Using fMRI, GTA, and ddRADseq methods of analysis provided us with three unique angles from which to more wholistically study the prairie vole. Overall, our findings have further confirmed that the prairie vole is a powerful transgenerational animal model