Inducing Partner Preference in Mice by Chemogenetic Stimulation of CA2 Hippocampal Subfield

Cymerblit‐Sabba, Adi; Smith, A. R.; Avram, Sarah K. Williams; Stackmann, Michelle; Korgan, Austin C.; Tickerhoof, Maria C.; Young, W. Scott

doi:10.3389/fnmol.2020.00061

Cited by 11 publications

(7 citation statements)

References 35 publications

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“…The formation of selective social relationships is a particular hallmark of both human and prairie vole societies. Such relationships are difficult to study in traditional lab rodents because mice, rats, and other rodents typically do not form preferences for known peers or mates ( Triana-Del Rio et al, 2015 ; Schweinfurth et al, 2017 ; Beery et al, 2018 ; Cymerblit-Sabba et al, 2020 ; Insel et al, 2020 ; Beery and Shambaugh, 2021 ). In species that form specific relationships, selectivity may be based on reward and prosocial motivation toward specific individuals, or on avoidance (fear, aggression) of unfamiliar individuals.…”

Section: Introductionmentioning

confidence: 99%

Social selectivity and social motivation in voles

Beery

Lopez

Blandino

et al. 2021

eLife

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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 (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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Section: Introductionmentioning

confidence: 99%

Social selectivity and social motivation in voles

Beery

Lopez

Blandino

et al. 2021

eLife

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“…Previously, we showed that loss of the Avpr1b from the pyramidal neurons of the CA2 results in inability of mice to recognize a familiar conspecific 6–7 . We also described an enhancement of social recognition following activation of the paraventricular nucleus (PVN) terminals in CA2, mediated by the Avpr1b 2 and, further, we were able to induce atypical partner preference behavior in mice through similar activation of the same neuronal pathway 8 .…”

Section: Introductionmentioning

confidence: 64%

Simultaneous Knockouts of the Oxytocin and Vasopressin 1b Receptors in Hippocampal CA2 Impair Social Memory

Cymerblit‐Sabba¹,

Walsh²,

Duan³

et al. 2023

Preprint

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Oxytocin (Oxt) and vasopressin (Avp) are two neuropeptides with many central actions related to social cognition. The oxytocin (Oxtr) and vasopressin 1b (Avpr1b) receptors are co-expressed in the pyramidal neurons of the hippocampal subfield CA2 and are known to play a critical role in social memory formation. How the neuropeptides perform this function in this region is not fully understood. Here, we report the behavioral effects of a life-long conditional removal (knockout, KO) of either the Oxtr alone or both Avpr1b and Oxtr from the pyramidal neurons of CA2 as well as the resultant changes in synaptic transmission within the different fields of the hippocampus. Surprisingly, the removal of both receptors results in mice that are unable to habituate to a familiar female presented for short duration over short intervals but are able to recognize and discriminate females when presented for a longer duration over a longer interval. Importantly, these double KO mice were unable to discriminate between a male littermate and a novel male. Synaptic transmission between CA3 and CA2 is enhanced in these mice, suggesting a compensatory mechanism is activated to make up for the loss of the receptors. Overall, our results demonstrate that co-expression of the receptors in CA2 is necessary to allow intact social memory processing.

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“…Opposite-sex partner preference has also been assessed across a range of rodents of differing mating systems, including prairie voles, montane voles (Insel & Hulihan, 1995), meadow voles (Parker, Phillips, & Lee, 2001), California mice (Kowalczyk, Davila, & Trainor, 2018), mice (Cymerblit-Sabba et al, 2020), striped mice (Garnier & Schradin, 2019), and three gerbil species (Tchabovsky et al, 2019). Of these, partner preferences were most evident in prairie voles, meadow voles, female striped mice, and male Mongolian gerbils under control conditions.…”

Section: Subject Considerations: Other Speciesmentioning

confidence: 99%

“…Of these, partner preferences were most evident in prairie voles, meadow voles, female striped mice, and male Mongolian gerbils under control conditions. Other species, such as mice, showed partner preferences following specific neural manipulations (Cymerblit‐Sabba et al., 2020). Partner preference for a familiar mate has also been assessed with varied testing setups in other taxonomic groups including birds (zebra finches; Kingsbury & Goodson, 2014; Smiley, Vahaba, & Tomaszycki, 2012) and primates (marmosets; Carp et al., 2016).…”

Section: Commentarymentioning

confidence: 99%

Familiarity and Mate Preference Assessment with the Partner Preference Test

Beery

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

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Inducing Partner Preference in Mice by Chemogenetic Stimulation of CA2 Hippocampal Subfield

Cited by 11 publications

References 35 publications

Social selectivity and social motivation in voles

Social selectivity and social motivation in voles

Simultaneous Knockouts of the Oxytocin and Vasopressin 1b Receptors in Hippocampal CA2 Impair Social Memory

Familiarity and Mate Preference Assessment with the Partner Preference Test

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