Rewritable fidelity: How repeated pairings and age influence subsequent pair-bond formation in male prairie voles

Abstract

The prairie vole has proven a valuable animal model for the neurobiological study of social monogamy and pair bonding. Previous research has focused almost exclusively on virgin prairie voles forming pair-bonds for the first time -a paradigm with limited relevance to human social behavior. In the present study, we used stud males to assess the impact of repeated pair-bond formation and dissolution on the behaviors and neurobiology relevant to subsequent pair-bond formation. Stud males were tested for behavioral and neurobiological e ffects of repeated pairbonding after the 1st, 5th, and 10th pairing. Aged breeder males that experienced minimal pairbond dissolution were included to control for the effects of aging. Results showed that male prairie voles readily form new pair-bonds after repeated pair-bond dissolution. In terms of social monogamy, old age was associated with males spending less time in close social contact with unfamiliar females. There were no effects of age nor number of lifetime pairings on depressivelike behavior or paternal behavior toward pups. Within the brain, the patterns of oxytocin (OTR) and vasopressin type 1a (V1aR) receptors were largely unaffected, with the following exceptions: 1) males with only a single pairing had higher OTR densities in the paraventricular thalamus and bed nucleus of the stria terminalis; 2) there was an age-related increase in the density of OTR in the caudate putamen and an age-related decline in the density of V1aR in the cortical amygdala. The present findings have translational relevance to human social behavior in the context of aging and social experience.

How prior pair-bonding experience affects future bonding behavior in monogamous prairie voles

“…It is worth noting that at a superficial level, our results and those of Kenkel et al (2019), which indicate that preference formation is common even following multiple pairings, may seem at odds with reports that only ~20% of male and female prairie voles re-pair in the wild (Carter and Figure 4. Effects of mating latency on partner preference.…”

“…Thus, these conditions were behaviorally equivalent with respect to the behaviors displayed towards their first partner. Similar to previous reports by Kenkel et al (2019), we found that voles in all conditions were capable of showing a preference for their second partner within 3 days of pairing (short-term; 48 Hour p = 0.022, 2 Week p = 0.003, 4 Week p = 0.075 (but see significant distance data), Fig. 3: A, D, G).…”

“…A prior study opportunistically used "stud males," or male voles that were known to reliably mate, to show that that male prairie voles can demonstrate a partner preference even following pairing and mating with up to 10 females (Kenkel et al, 2019). Our study builds on this initial observation in three key ways.…”

“…In the wild, prairie voles occasionally re-pair; ~20% will take a new partner (Carter and Getz, 1993). Recent laboratory studies suggest that most male voles will form a partner preference, a behavioral proxy for a pair bond, regardless of prior pairing, even after being sequentially paired and mating with up to 10 females (Kenkel et al, 2019). While this demonstrates that previous pairing/mating does not negate the ability to form future bonds, a number of questions remain regarding the role of previous experience in subsequent bond formation and expression.…”

Familiarity and Mate Preference Assessment with the Partner Preference Test

“…The extended‐duration partner preference test has also been adapted to assess preference for individuals exhibiting different characteristics related to but beyond basic familiarity. For example, the test has been used to test preference for new versus former partners in prairie voles (Harbert, Pellegrini, Gordon, & Donaldson, 2020), preference for huddling with a group versus a single partner in same‐sex meadow voles (Ondrasek et al., 2015), preference for gonadally intact versus gonadectomized subjects, preference for same‐ versus opposite‐sex individuals (DeVries et al., 1997), and changes with age and repeated pairing (Kenkel et al., 2019).…”