Septal oxytocin administration impairs peer affiliation via V1a receptors in female meadow voles

Anacker, Allison M.J.; Christensen, Jennifer D.; LaFlamme, Elyssa M.; Grunberg, Diana; Beery, Annaliese K.

doi:10.1016/j.psyneuen.2016.02.025

Cited by 39 publications

(36 citation statements)

References 68 publications

(105 reference statements)

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“…PPTs were conducted as described previously (Ahern et al, 2009 ; Anacker et al, 2016a , b ), using the same apparatuses as the SPT. Familiar and novel social stimulus animals were tethered at opposite ends of the apparatus (Figure 1B ).…”

Section: Methodsmentioning

confidence: 99%

“…The PPT has been used extensively to assess how different manipulations alter formation and maintenance of preferences for a mate in monogamous prairie voles and to a lesser degree in other monogamous species (Ahern et al, 2009 ; Kingsbury and Goodson, 2014 ; Carp et al, 2016 ). The PPT is also used to assess factors affecting social preferences for same-sex peers in meadow voles (Beery and Zucker, 2010 ; Anacker et al, 2016a , b ), prairie voles (DeVries et al, 1997 ), and occasionally other rodents (e.g., Triana-Del Rio et al, 2011 ). One study has examined long-term social preferences of female mice during an 18 h three-chambered social choice test with stimulus mice housed behind wire mesh (Harrison et al, 2016 ).…”

Section: Introductionmentioning

confidence: 99%

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Specificity in Sociality: Mice and Prairie Voles Exhibit Different Patterns of Peer Affiliation

Beery

Christensen

Lee

et al. 2018

Front. Behav. Neurosci.

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Social behavior is often described as a unified concept, but highly social (group-living) species exhibit distinct social structures and may make different social decisions. Prairie voles (Microtus ochrogaster) are socially monogamous rodents that often reside in extended family groups, and exhibit robust preferences for familiar social partners (same- and opposite-sex) during extended choice tests, although short-term preferences are not known. Mice (Mus musculus) are gregarious and colonial, but in brief laboratory tests of social preference they typically prefer social novelty. This preference for novel vs. familiar peers may represent a species-specific difference in social decision-making between mice and prairie voles. However, the tests used to measure preferences in each species differ markedly in duration and degree of contact, such that the behaviors cannot be directly compared. We assessed whether social preferences for novelty or familiarity differed between mice and prairie voles of both sexes when assessed with matching protocols: the sociability/social preference test (SPT) typically used in mice (short, no direct contact), and the partner preference test (PPT) used in voles (long, direct contact). A subset of voles also underwent a PPT using barriers (long, no direct contact). In the short SPT, behavior did not differ between species. In the longer test, pronounced partner preferences emerged in prairie voles, but mice exhibited no social preferences and rarely huddled. No sex differences were evident in either test. Direct physical contact was required for partner preferences in huddling time in voles, but preference for the partner chamber was evident with or without contact. Both prairie voles and mice are social, but they exhibit important differences in the specificity and extent of their social behavior. While mice are often used to study social approach and other behaviors, voles are a more suitable species for the study of selective social relationships. Consideration of these differences will be important for studies examining the neural mechanisms supporting different kinds of peer social behavior.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Specificity in Sociality: Mice and Prairie Voles Exhibit Different Patterns of Peer Affiliation

Beery

Christensen

Lee

et al. 2018

Front. Behav. Neurosci.

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“…Oxytocin (OT) is a neuropeptide that plays a broad role in modulating the social repertoire of species across the animal kingdom (Insel, 1992;Donaldson and Young, 2008;Neumann, 2008;Bales and Perkeybile, 2012;Carter, 2014;Tabbaa et al, 2016). To date, the OT system has been associated with social recognition (Oettl et al, 2016), social learning and memory (Ferguson et al, 2001;Choe et al, 2015), social reward (Dölen et al, 2013;Young et al, 2014), attachment formation (Insel, 1992;Wang and Aragona, 2004;Young and Wang, 2004), sexual behavior (Bitran and Hull, 1987;Yanagimoto et al, 1996;Caquineau et al, 2006;Ludwig and Leng, 2006), parental care (Pedersen and Prange, 1979;Bell et al, 2014;Marlin et al, 2015;Scott et al, 2015;Bales and Saltzman, 2016;Mitre et al, 2016), and aggression (Ebner et al, 2000;Anacker et al, 2016;Ne'eman et al, 2016;Zimmermann et al, 2016). The pervasive influence of the OT system extends to social contexts of both positive and negative valence and may play a critical role in the regulation of processes that are fundamental to the expression of all social behaviors (Choe et al, 2015;Nardou et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Social Stimuli Induce Activation of Oxytocin Neurons Within the Paraventricular Nucleus of the Hypothalamus to Promote Social Behavior in Male Mice

Resendez¹,

Namboodiri²,

Otis³

et al. 2020

J. Neurosci.

111

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Oxytocin (OT) is critical for the expression of social behavior across a wide array of species; however, the role of this system in the encoding of socially relevant information is not well understood. In the present study, we show that chemogenetic activation of OT neurons within the paraventricular nucleus of the hypothalamus (PVH) of male mice (OT-Ires-Cre) enhanced social investigation during a social choice test, while chemogenetic inhibition of these neurons abolished typical social preferences. These data suggest that activation of the OT system is necessary to direct behavior preferentially toward social stimuli. To determine whether the presence of a social stimulus is sufficient to induce activation of PVH-OT neurons, we performed the first definitive recording of OT neurons in awake mice using two-photon calcium imaging. These recordings demonstrate that social stimuli activate PVH-OT neurons and that these neurons differentially encode social and nonsocial stimuli, suggesting that PVH-OT neurons may act to convey social salience of environmental stimuli. Finally, an attenuation of social salience is associated with social disorders, such as autism. We therefore also examined possible OT system dysfunction in a mouse model of autism, Shank3b knockout (KO) mice. Male Shank3b KO mice showed a marked reduction in PVH-OT neuron number and administration of an OT receptor agonist improved social deficits. Overall, these data suggest that the presence of a social stimulus induces activation of the PVH-OT neurons to promote adaptive social behavior responses.

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“…The three-hour duration of the test allows habituation to the test configuration and further promotes resting and social contact. This test was originally developed to assess opposite-sex mate preferences in prairie voles, but has since been extended to same-sex partner preferences in prairie voles (DeVries et al, 1997b; Beery et al, 2018) and meadow voles (Anacker et al, 2016a, 2016b; Beery et al, 2009, 2008; Beery and Zucker, 2010; Ondrasek et al, 2015; Parker and Lee, 2003), as well as other rodents (degus: Shambaugh, Insel and Beery personal communication ; mice: Beery et al, 2018).…”

Section: Meadow Voles: Behaviormentioning

confidence: 99%

Frank Beach award winner: Neuroendocrinology of group living

Beery

2019

Hormones and Behavior

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Why do members of some species live in groups while others are solitary? Group living (sociality) has often been studied from an evolutionary perspective, but less is known about the neurobiology of affiliation outside the realms of mating and parenting. Colonial species offer a valuable opportunity to study nonsexual affiliative behavior between adult peers. Meadow voles (Microtus pennsylvanicus) display environmentally induced variation in social behavior, maintaining exclusive territories in summer months, but living in social groups in winter. Research on peer relationships in female meadow voles demonstrates that these selective preferences are mediated differently than mate relationships in socially monogamous prairie voles, but are also impacted by oxytocin and HPA axis signaling. This review addresses day-length dependent variation in physiology and behavior, and presents the current understanding of the mechanisms supporting selective social relationships in meadow voles, with connections to lessons from other species.

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Septal oxytocin administration impairs peer affiliation via V1a receptors in female meadow voles

Cited by 39 publications

References 68 publications

Specificity in Sociality: Mice and Prairie Voles Exhibit Different Patterns of Peer Affiliation

Specificity in Sociality: Mice and Prairie Voles Exhibit Different Patterns of Peer Affiliation

Social Stimuli Induce Activation of Oxytocin Neurons Within the Paraventricular Nucleus of the Hypothalamus to Promote Social Behavior in Male Mice

Frank Beach award winner: Neuroendocrinology of group living

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