The role of dopamine signaling in prairie vole peer relationships

Lopez

Blandino

et al. 2021

Preprint

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Selective relationships are fundamental to humans and many other animals, but relationships between mates, family members, or peers may be mediated differently. We examined connections between social reward and social selectivity, aggression, and oxytocin receptor signaling pathways in rodents that naturally form enduring, selective relationships with mates and peers (prairie voles) or peers (meadow voles). Female prairie and meadow voles worked harder to access familiar vs. unfamiliar individuals, regardless of sex, and huddled extensively with familiar subjects. Male prairie voles also displayed strongly selective huddling preferences for familiar animals, but worked hardest to repeatedly access females vs. males, with no difference in effort by familiarity. This demonstrates a fundamental disconnect between motivation and social selectivity in males, and reveals a striking sex difference in pathways underlying social monogamy. Meadow voles exhibited social preferences but low social motivation, consistent with tolerance rather than reward supporting social groups in this species. Natural variation in oxytocin receptor genotype was associated with oxytocin receptor density, and both genotype and receptor binding predicted individual variation in prosocial and aggressive behaviors. These results provide a basis for understanding species, sex, and individual differences in the mechanisms underlying the role of social reward in social preference.

Section: Introductionmentioning

confidence: 88%

Social selectivity and social motivation in voles

Lopez

Blandino

et al. 2021

Preprint

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“…The same‐sex peer partner preference test is regularly used in meadow voles, which exhibit group living and peer social preferences in winter in the wild and under conditions of short (winter‐like) photoperiods in the laboratory (Beery, 2019). This test has been used extensively to probe the basis of nonreproductive social relationships in both adult meadow voles (Anacker, Christensen, LaFlamme, Grunberg, & Beery, 2016; Anacker, Reitz, Goodwin, & Beery, 2016; Beery & Zucker, 2010; Beery et al., 2008; Beery, Vahaba, & Grunberg, 2014; Goodwin, Lopez, Lee, & Beery, 2019; Lee & Beery, 2021; Lee et al., 2019; Ondrasek et al., 2015; Parker & Lee, 2003) and prairie voles (Beery et al., 2018; DeVries et al., 1997; Goodwin et al., 2019; Lee & Beery, 2021; Lee et al., 2019). The peer partner preference test differs from the opposite‐sex partner preference test only in that all three subjects are of the same sex.…”

Section: Commentarymentioning

confidence: 99%

“…Figure 2 Sample partner preference test data and timeline analysis. Sample data are from female prairie voles tested with their male partner and a male stranger (data from Lee & Beery, 2021).…”

mentioning

confidence: 99%

Familiarity and Mate Preference Assessment with the Partner Preference Test

2021

Current Protocols

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In contrast to traditional laboratory animals, prairie voles form socially monogamous partnerships in the wild and exhibit lasting social preferences for familiar individuals—both mates and same‐sex peers—in the laboratory. Decades of research into the mechanisms supporting pair bonding behavior have made prairie voles an important model organism for the study of social relationships. The partner preference test is a laboratory test of familiarity preference that takes place over an extended interval (typically 3 hr), during which test subjects can directly interact with conspecifics and often engage in resting side‐by‐side contact (i.e., huddling). The use of this test has enabled study of the neural pathways and mechanisms involved in promoting or impairing relationship formation. The tendency to form partner preferences is also used as a behavioral indicator of the effects of early life experiences and environmental exposures. While this test was developed to assess the extent of social preference for mates in prairie voles, it has been adapted for use in other social contexts and in multiple other species. This article provides instructions for conducting the classic partner preference test, as well as variations including same‐sex “peer” partner preference tests. The effects of several protocol variations are examined, including duration of cohousing, separation interval, use of tethers versus barriers, linear versus branched apparatus configuration, and duration of the test. The roles of social variables including sex of the focal individual, sex of conspecifics, reproductive state, and use of the test in other species are then considered. Finally, sample data are provided along with discussion of scoring and statistical analysis of partner preference tests. © 2021 Wiley Periodicals LLC. Basic Protocol: Partner preference test Support Protocol: Behavioral scoring

“…The use of the same-sex, peer implementation of the partner preference test (referred to as the same-sex PPT, or as herein: peer PPT) provides a standardized assessment of familiarity preferences which do not emerge during brief preference tests (Beery et al, 2018). We have used the peer PPT in our lab for over a decade in studies of day-length mediated variation in group living (sociality) in meadow voles (Beery et al, 2008b(Beery et al, , 2009(Beery et al, , 2014Beery and Zucker, 2010;Anacker et al, 2016a,b;Goodwin et al, 2019;Lee et al, 2019;Lee and Beery, 2021). More recently we have assessed same-sex peer partner preferences in a variety of rodent species that live in groups but differ in the nature of their social system (Table 1).…”

Section: Introductionmentioning

confidence: 99%

Comparative Assessment of Familiarity/Novelty Preferences in Rodents

Front. Behav. Neurosci.

Shambaugh

2021

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Sociality—i.e., life in social groups—has evolved many times in rodents, and there is considerable variation in the nature of these groups. While many species-typical behaviors have been described in field settings, the use of consistent behavioral assays in the laboratory provides key data for comparisons across species. The preference for interaction with familiar or novel individuals is an important dimension of social behavior. Familiarity preference, in particular, may be associated with more closed, less flexible social groups. The dimension from selectivity to gregariousness has been used as a factor in classification of social group types. Laboratory tests of social choice range from brief (10 minutes) to extended (e.g., 3 hours). As familiarity preferences typically need long testing intervals to manifest, we used 3-hour peer partner preference tests to test for the presence of familiarity preferences in same-sex cage-mates and strangers in rats. We then conducted an aggregated analysis of familiarity preferences across multiple rodent species (adult male and female rats, mice, prairie voles, meadow voles, and female degus) tested with the same protocol. We found a high degree of consistency within species across data sets, supporting the existence of strong, species-typical familiarity preferences in prairie voles and meadow voles, and a lack of familiarity preferences in other species tested. Sociability, or total time spent near conspecifics, was unrelated to selectivity in social preference. These findings provide important background for interpreting the neurobiological mechanisms involved in social behavior in these species.