Emergent intra‐pair sex differences and organized behavior in pair bonded prairie voles (Microtus ochrogaster)

Abstract

In pair bonding animals, coordinated behavior between partners is required for the pair to accomplish shared goals such as raising young. Despite this, experimental designs rarely assess the behavior of both partners within a bonded pair. Thus, we lack an understanding of the interdependent behavioral dynamics between partners that likely facilitate relationship success. To identify intra-pair behavioral correlates of pair bonding, we used socially monogamous prairie voles (Microtus ochrogaster) and tested both partners using social choice and non-choice tests at short-and long-term pairing timepoints.Females developed a preference for their partner more rapidly than males, with preference driven by different behaviors in each sex. Further, as bonds matured, intra-pair behavioral sex differences and organized behavior emerged-females consistently huddled more with their partner than males did regardless of overall intra-pair affiliation levels. When animals were allowed to freely interact with a partner or a novel vole in sequential free interaction tests, pairs spent more time interacting together than either animal did with a novel vole, consistent with partner preference in the more commonly employed choice test. Total pair interaction in freely moving voles was correlated with female, but not male, behavior. Via a social operant paradigm, we found that pairbonded females, but not males, are more motivated to access and huddle with their partner than a novel vole. Together, our data indicate that as pair bonds mature, sex differences and organized behavior emerge within pairs, and that these intra-pair behavioral changes are likely organized and driven by the female animal.

Nucleus accumbens dopamine release reflects the selective nature of pair bonds

“…We performed fiber photometry to measure GRAB DA -mediated fluorescence as a proxy for extracellular dopamine levels in the nucleus accumbens of voles engaged in operant responding and reward consumption (Fig 1A - C) ( 17 ). We used a previously established social operant task in voles ( 15 ). Voles learned to initially associate rewards with lever pressing through food delivery (Fig S1A - D) before being presented with separate levers that provided transient access to a tethered partner and novel animal (Fig 1D - F).…”

“…This task is uniquely advantageous in that it separates the appetitive aspect of social reward, reflected in lever pressing and cues predicting social access, from the consummatory aspect of physical social interaction. Furthermore, this task elicits comparable degrees of lever-pressing for both partner and novel voles ( 15 ). Using fiber photometric recordings of the fluorescent dopamine sensor, GRAB DA , we found that anticipation of partner reunion, as well as partner interaction, results in enhanced nucleus accumbens dopamine release compared with the same events directed towards a novel opposite-sex vole.…”

“…In this test, a pair bonded vole will choose to spend most of their time with their mating partner compared with a novel opposite sex vole or time spent alone (12,13). Similarly, voles will lever-press to gain transient access to their partner in an operant task (14)(15)(16). However, it remains unknown how real-time dopamine release dynamics contribute to the selective nature of pair bonds and potentially drive partner-directed versus novel-vole-directed behaviors.…”

Naked Mole-Rat Social Phenotypes Vary in Investigative and Aggressive Behavior in a Laboratory Partner Preference Paradigm

“…The formation of stable social groups contributes both to the selectiveness for familiar peers as well as the aggression toward unfamiliar conspecifics, especially following mating (Carter and Getz, 1993;Lee et al, 2019). While there are subtle sex differences in partner preference development, both male and female prairie voles show strong selectivity in their interactions by spending more time with familiar rather than unfamiliar same-sex conspecifics (Brusman et al, 2022). Prairie voles are also often aggressive toward unfamiliar same-sex individuals (Lee et al, 2019;Vahaba et al, 2021).…”

Deepening the understanding of social bonding and dynamics of social interactions

“…They provide critical evidence against the idea of potential monomorphism in pair-bonding behaviors in these socially monogamous species. The article by Brusman et al 6 compares indices of pair-bonding in the standard "choice" partner preference test 7,8 and a novel modified non-choice test across two time points between male and female prairie voles.…”