Social selectivity and social motivation in voles
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Evaluation Summary:
This paper introduces a new method to measure motivation to engage with familiar or unfamiliar individuals in prairie voles, a widely used animal model system for studying social relationships. The authors show that female prairie voles will work harder to access both familiar pair-bonded males or familiar females. In contrast, male prairie voles will work to access both pair-bonded females as well as unfamiliar females. These results cast a new light on decades of work based partner-preference tests that assess pair bonds that do not assess the role of motivation.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #3 agreed to share their name with the authors.)
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Abstract
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 (monogamous prairie voles) or peers (group-living meadow voles). Female prairie and meadow voles worked harder to access familiar versus unfamiliar individuals, regardless of sex, and huddled extensively with familiar subjects. Male prairie voles displayed strongly selective huddling preferences for familiar animals, but only worked harder to repeatedly access females versus males, with no difference in effort by familiarity. This reveals a striking sex difference in pathways underlying social monogamy and demonstrates a fundamental disconnect between motivation and social selectivity in males—a distinction not detected by the partner preference test. 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 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.
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Author Response:
Reviewer #2 (Public Review):
The authors used an operant task in voles to assess preferences for social relationships and whether these preferences differed by sex and species. They also correlated some outcomes with oxytocin receptor binding.
A strength of the paper is the use of the vole models which allow comparisons between socially monogamous (prairie voles) vs. promiscuous breeders (meadow voles). Because prairie voles show a stronger preference for peers and mates than many other rodent species, they are a great model to assess selective relationships. The other major strength of this paper is the use of the operant procedure to assess preference. To my knowledge, this is the first time this procedure has been used to assess social reward in a monogamous species, and it has advantages over place preference …
Author Response:
Reviewer #2 (Public Review):
The authors used an operant task in voles to assess preferences for social relationships and whether these preferences differed by sex and species. They also correlated some outcomes with oxytocin receptor binding.
A strength of the paper is the use of the vole models which allow comparisons between socially monogamous (prairie voles) vs. promiscuous breeders (meadow voles). Because prairie voles show a stronger preference for peers and mates than many other rodent species, they are a great model to assess selective relationships. The other major strength of this paper is the use of the operant procedure to assess preference. To my knowledge, this is the first time this procedure has been used to assess social reward in a monogamous species, and it has advantages over place preference procedures.
A weakness of the paper is the omission of groups from certain manipulations. Male meadow voles were excluded from the operant procedure and all male data was excluded from oxytocin receptor analysis with little rationale. This limits some of the conclusions that can be made about males in the study. Additionally, some experimental design details were missing. A subset of rats went through extinction. However, it was unclear whether those used for oxytocin receptor analysis went through extinction or not (or were from both conditions). The biochemical analysis also assessed the effect of oxytocin receptor genotype, replicating the effect that C allele carriers have higher oxytocin receptor binding in specific brain regions. However, the analysis of this genotype's effect on behavior was limited due, presumably, to power issues with most measures. Thus, conclusions regarding genotype were limited. Finally, there was a missed opportunity to do a progressive ratio test to better assess motivation for the partner rat.
The operant task and the subsequent behavioral results will be useful for the field, but the design issues somewhat limit impact. However, assessing the formation of selective relationships and using the vole model is innovative.
Regarding testing protocol, we exclusively used a progressive ratio schedule (PR-1) in all testing phases of our study. This has been emphasized throughout the manuscript, and hopefully obviates any concerns about limits to the interpretation of fixed ratio studies.
Excellent point about the need for more detail on inclusion of each sex. Information has now been added as to why males were not tested in two aspects of the study. Males were not included in the meadow vole portion of the study because only females of this species show pronounced seasonal differences in affiliative behavior. We have added the text: “Because the seasonal transition from solitary to social is most pronounced in female meadow voles in the field and laboratory (Madison and McShea, 1987; Beery et al., 2009), only females of this species were used.” We initially planned to include males in oxytocin receptor assays, but when early results suggested males did not work harder to access familiar females, we retained later study males to test a two-choice variant of the social operant setup (instead of collecting their brains at the conclusion of this study). That pilot led us to conduct a new study using the two-choice operant apparatus (in review), and the tissues from that second study could enable a similar analysis in both male and female brains.
Additional details have been added regarding which voles underwent extinction, and we have removed the genotype data from the manuscript as requested.
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Evaluation Summary:
This paper introduces a new method to measure motivation to engage with familiar or unfamiliar individuals in prairie voles, a widely used animal model system for studying social relationships. The authors show that female prairie voles will work harder to access both familiar pair-bonded males or familiar females. In contrast, male prairie voles will work to access both pair-bonded females as well as unfamiliar females. These results cast a new light on decades of work based partner-preference tests that assess pair bonds that do not assess the role of motivation.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #3 agreed to share their name with the authors.)
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Reviewer #1 (Public Review):
In this manuscript the authors introduce a novel operant conditioning paradigm for prairie voles that assesses motivation of individuals to access pair-bonded partners versus unfamiliar social individuals. Prairie voles are an important model species for studying social relationships, and a large group of investigators have settled on standard methodology for partner preference tests to assess pair bonds. As the authors highlight, partner preference tests (a current gold standard in the field) cannot distinguish between motivation to associate with a pair-mate or avoidance of an unfamiliar individual. Operant training for social stimuli has only been done a handful of times, and never used to study social relationships in an animal model. The authors also combined lever pressing data with ethological scoring …
Reviewer #1 (Public Review):
In this manuscript the authors introduce a novel operant conditioning paradigm for prairie voles that assesses motivation of individuals to access pair-bonded partners versus unfamiliar social individuals. Prairie voles are an important model species for studying social relationships, and a large group of investigators have settled on standard methodology for partner preference tests to assess pair bonds. As the authors highlight, partner preference tests (a current gold standard in the field) cannot distinguish between motivation to associate with a pair-mate or avoidance of an unfamiliar individual. Operant training for social stimuli has only been done a handful of times, and never used to study social relationships in an animal model. The authors also combined lever pressing data with ethological scoring of behavior when focal animals received access to stimulus animals. Their results show that while female prairie voles lever press more for familiar individuals (both a male mate or same-sex cagemate), males lever press more for access to females regardless of familiarity. Lever pressing for an empty compartment was positively correlated with pressing for an unfamiliar individual, suggesting that lever presses for strangers might be spontaneous. In contrast when measuring huddling behavior (the standard measure in partner-preference tests), both males and females huddled more with familiar individuals. The experiments are rigorously conducted and proper extinction controls are included to demonstrate the effectiveness of the method. The authors' results highlight how partner-preference tests capture only a fraction of the behavioral processes involved in pair bonding in prairie voles and make an important contribution to our understanding of the processes involved in maintenance of social relationships.
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Reviewer #2 (Public Review):
The authors used an operant task in voles to assess preferences for social relationships and whether these preferences differed by sex and species. They also correlated some outcomes with oxytocin receptor binding.
A strength of the paper is the use of the vole models which allow comparisons between socially monogamous (prairie voles) vs. promiscuous breeders (meadow voles). Because prairie voles show a stronger preference for peers and mates than many other rodent species, they are a great model to assess selective relationships. The other major strength of this paper is the use of the operant procedure to assess preference. To my knowledge, this is the first time this procedure has been used to assess social reward in a monogamous species, and it has advantages over place preference procedures.
A weakness …
Reviewer #2 (Public Review):
The authors used an operant task in voles to assess preferences for social relationships and whether these preferences differed by sex and species. They also correlated some outcomes with oxytocin receptor binding.
A strength of the paper is the use of the vole models which allow comparisons between socially monogamous (prairie voles) vs. promiscuous breeders (meadow voles). Because prairie voles show a stronger preference for peers and mates than many other rodent species, they are a great model to assess selective relationships. The other major strength of this paper is the use of the operant procedure to assess preference. To my knowledge, this is the first time this procedure has been used to assess social reward in a monogamous species, and it has advantages over place preference procedures.
A weakness of the paper is the omission of groups from certain manipulations. Male meadow voles were excluded from the operant procedure and all male data was excluded from oxytocin receptor analysis with little rationale. This limits some of the conclusions that can be made about males in the study. Additionally, some experimental design details were missing. A subset of rats went through extinction. However, it was unclear whether those used for oxytocin receptor analysis went through extinction or not (or were from both conditions). The biochemical analysis also assessed the effect of oxytocin receptor genotype, replicating the effect that C allele carriers have higher oxytocin receptor binding in specific brain regions. However, the analysis of this genotype's effect on behavior was limited due, presumably, to power issues with most measures. Thus, conclusions regarding genotype were limited. Finally, there was a missed opportunity to do a progressive ratio test to better assess motivation for the partner rat.
The operant task and the subsequent behavioral results will be useful for the field, but the design issues somewhat limit impact. However, assessing the formation of selective relationships and using the vole model is innovative.
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Reviewer #3 (Public Review):
In this paper, the authors attempted to disentangle social preference and social motivation in two different vole species (monogamous prairie voles and polygynous meadow voles) and in different types of relationships (same-sex and opposite-sex). They also examined the role of sex differences in these questions. Finally, they examined a single nucleotide polymorphism in the oxytocin receptor gene, and its role in predicting oxytocin receptor density and social behavior.
Strengths: The authors have performed very elegant and detailed behavioral tests and analyses. The focus on sex differences and relationship type, and the inclusion of same-sex pairs, is a major strength. The graphs are nicely done and I especially appreciate the individual data points in some graphs and the way that they are connected, so we …
Reviewer #3 (Public Review):
In this paper, the authors attempted to disentangle social preference and social motivation in two different vole species (monogamous prairie voles and polygynous meadow voles) and in different types of relationships (same-sex and opposite-sex). They also examined the role of sex differences in these questions. Finally, they examined a single nucleotide polymorphism in the oxytocin receptor gene, and its role in predicting oxytocin receptor density and social behavior.
Strengths: The authors have performed very elegant and detailed behavioral tests and analyses. The focus on sex differences and relationship type, and the inclusion of same-sex pairs, is a major strength. The graphs are nicely done and I especially appreciate the individual data points in some graphs and the way that they are connected, so we can see how the same individual performed in different conditions. The authors included a food control in the rewards experiments, showing that their results were specific to social reward.
Weaknesses: At least one part of the study (the oxytocin receptor density) was carried out only in females. It is also not clear what broader significance the role of this particular single nucleotide polymorphism of the oxytocin receptor might have; for example, whether this same polymorphism is found in other species including humans. Some experiments had relatively small sample sizes.
The authors did achieve their aims and the results supported their conclusions.
Studies on same-sex relationships are still very rare in behavioral neuroscience, and in the study of animal behavior in general. It is quite significant that these authors have shown that female prairie voles are just as motivated to gain access to a same-sex partner as an opposite-sex partner. While most of these methods have been published elsewhere already, this paper is a model of attention to detail in the study of behavior.
In addition, the prairie vole vs. meadow vole comparison is now a classic one in social neuroscience, and this paper adds depth to the interpretation of differences between the species.
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