scholarly journals Social selectivity and social motivation in voles

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Annaliese K Beery ◽  
Sarah A Lopez ◽  
Katrina L Blandino ◽  
Nicole S Lee ◽  
Natalie S Bourdon

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 vs. 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 vs. 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.

2021 ◽  
Author(s):  
Annaliese K Beery ◽  
Sarah A Lopez ◽  
Katrina L Blandino ◽  
Nicole S Lee ◽  
Natalie S Bourdon ◽  
...  

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.


1997 ◽  
Vol 75 (2) ◽  
pp. 295-301 ◽  
Author(s):  
A. Courtney DeVries ◽  
Camron L. Johnson ◽  
C. Sue Carter

The physiological mechanisms influencing group cohesion and social preferences are largely unstudied in prairie voles (Microtus ochrogaster). In nature, prairie vole family groups usually consist of an adult male and female breeding pair, one or more litters of their offspring, and occasionally unrelated adults. Pair bonds, defined by heterosexual preferences, develop in male and female prairie voles following cohabitation or mating. However, social preferences between members of the same sex also may be important to the maintenance of communal groups. In the present study we compared the development of social preferences for conspecific strangers of the same sex versus preferences for the opposite sex, and examined the effect of the gonadal status of the stimulus animal on initial social preference. The present study revealed that reproductively naive males, but not females, showed initial preferences for partners of the opposite sex. In both sexes preferences for the opposite sex were not influenced by the presence or absence of gonadal hormones. Heterosexual and same-sex preferences for a familiar individual formed following 24 h of nonsexual cohabitation in both males and females. Male and female same-sex preferences, however, were no longer stable when the stranger in the preference test was of the opposite sex to the experimental animal. The development of same-sex preferences may help to maintain group cohesion, but same-sex preferences formed by cohabitation do not withstand the challenge of an opposite-sex stranger.


2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Shai Netser ◽  
Ana Meyer ◽  
Hen Magalnik ◽  
Asaph Zylbertal ◽  
Shani Haskal de la Zerda ◽  
...  

AbstractMice and rats are widely used to explore mechanisms of mammalian social behavior in health and disease, raising the question whether they actually differ in their social behavior. Here we address this question by directly comparing social investigation behavior between two mouse and rat strains used most frequently for behavioral studies and as models of neuropathological conditions: C57BL/6 J mice and Sprague Dawley (SD) rats. Employing novel experimental systems for behavioral analysis of both subjects and stimuli during the social preference test, we reveal marked differences in behavioral dynamics between the strains, suggesting stronger and faster induction of social motivation in SD rats. These different behavioral patterns, which correlate with distinctive c-Fos expression in social motivation-related brain areas, are modified by competition with non-social rewarding stimuli, in a strain-specific manner. Thus, these two strains differ in their social behavior, which should be taken into consideration when selecting an appropriate model organism.


2021 ◽  
Author(s):  
Daniel M Vahaba ◽  
Emily R Halstead ◽  
Zoe Donaldson ◽  
Todd H Ahern ◽  
Annaliese K Beery

The rewarding properties of social interactions facilitate relationship formation and maintenance. Prairie voles are one of the few laboratory species that form selective relationships, manifested as "partner preferences" for familiar partners versus strangers. While both sexes exhibit strong partner preferences, this similarity in outward behavior likely results from sex-specific neurobiological mechanisms. We recently used operant conditioning to demonstrate that females work harder for access to a familiar versus unfamiliar conspecific of either sex, while males worked equally hard for access to any female, indicating a key sex difference in social motivation. As tests were performed with one social target at a time, males might have experienced a ceiling effect, and familiar females might be more relatively rewarding in a choice scenario. Here we performed a social choice operant task in which voles could repeatedly lever-press to gain temporary access to either the chamber containing their mate or one containing a novel opposite-sex vole. Females worked hardest to access their mate, while males pressed at similar rates for either female. Individual male behavior was heterogeneous, congruent with multiple mating strategies in the wild. Voles exhibited preferences for favorable over unfavorable environments in a non-social operant task, indicating that lack of social preference does not reflect lack of discrimination between chambers. Oxytocin receptor genotype at the intronic SNP NT213739 replicated a prior association with stranger-directed aggression within the test. These findings suggest that convergent preference behavior in male and female voles results from sex-divergent pathways, particularly in the realm of social motivation.


2021 ◽  
Vol 15 ◽  
Author(s):  
Annaliese K. Beery ◽  
Katharine L. Shambaugh

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.


2019 ◽  
Vol 42 ◽  
Author(s):  
Teodora Gliga ◽  
Mayada Elsabbagh

Abstract Autistic individuals can be socially motivated. We disagree with the idea that self-report is sufficient to understand their social drive. Instead, we underscore evidence for typical non-verbal signatures of social reward during the early development of autistic individuals. Instead of focusing on whether or not social motivation is typical, research should investigate the factors that modulate social drives.


2020 ◽  
Author(s):  
Jessica Mow ◽  
Arti Gandhi ◽  
Daniel Fulford

Decreased social functioning and high levels of loneliness and social isolation are common in schizophrenia spectrum disorders (SSD), contributing to reduced quality of life. One key contributor to social impairment is low social motivation, which may stem from aberrant neural processing of socially rewarding or punishing stimuli. To summarize research on the neurobiology of social motivation in SSD, we performed a systematic literature review of neuroimaging studies involving the presentation of social stimuli intended to elicit feelings of reward and/or punishment. Across 11 studies meeting criteria, people with SSD demonstrated weaker modulation of brain activity in regions within a proposed social interaction network, including prefrontal, cingulate, and striatal regions, as well as the amygdala and insula. Firm conclusions regarding neural differences in SSD in these regions, as well as connections within networks, are limited due to conceptual and methodological inconsistencies across the available studies. We conclude by making recommendations for the study of social reward and punishment processing in SSD in future research.


Author(s):  
Tapan Mitra

The paper studies the sensitivity implications of the class of monotone social preference orders on infinite utility streams which satisfy the axioms of Equity (Finite Anonymity) and Stationarity (Independent Future). The principal result of this investigation is that representability of such preference orders implies a certain lack of sensitivity to the utility stream of any finite number of generations, which we refer to as ‘insensitivity to the present’. Our result points to a fundamental difficulty in implementing the sustainability principle, which requires intertemporal social preferences to reflect fairly the interests of the generations in the present and in the future.


BMC Genomics ◽  
2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Joel A. Tripp ◽  
Alejandro Berrio ◽  
Lisa A. McGraw ◽  
Mikhail V. Matz ◽  
Jamie K. Davis ◽  
...  

Abstract Background Pair bonding with a reproductive partner is rare among mammals but is an important feature of human social behavior. Decades of research on monogamous prairie voles (Microtus ochrogaster), along with comparative studies using the related non-bonding meadow vole (M. pennsylvanicus), have revealed many of the neural and molecular mechanisms necessary for pair-bond formation in that species. However, these studies have largely focused on just a few neuromodulatory systems. To test the hypothesis that neural gene expression differences underlie differential capacities to bond, we performed RNA-sequencing on tissue from three brain regions important for bonding and other social behaviors across bond-forming prairie voles and non-bonding meadow voles. We examined gene expression in the amygdala, hypothalamus, and combined ventral pallidum/nucleus accumbens in virgins and at three time points after mating to understand species differences in gene expression at baseline, in response to mating, and during bond formation. Results We first identified species and brain region as the factors most strongly associated with gene expression in our samples. Next, we found gene categories related to cell structure, translation, and metabolism that differed in expression across species in virgins, as well as categories associated with cell structure, synaptic and neuroendocrine signaling, and transcription and translation that varied among the focal regions in our study. Additionally, we identified genes that were differentially expressed across species after mating in each of our regions of interest. These include genes involved in regulating transcription, neuron structure, and synaptic plasticity. Finally, we identified modules of co-regulated genes that were strongly correlated with brain region in both species, and modules that were correlated with post-mating time points in prairie voles but not meadow voles. Conclusions These results reinforce the importance of pre-mating differences that confer the ability to form pair bonds in prairie voles but not promiscuous species such as meadow voles. Gene ontology analysis supports the hypothesis that pair-bond formation involves transcriptional regulation, and changes in neuronal structure. Together, our results expand knowledge of the genes involved in the pair bonding process and open new avenues of research in the molecular mechanisms of bond formation.


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