Oxytocin receptor density is associated with male mating tactics and social monogamy

Ophir, Alexander G.; Gessel, Ana; Zheng, Donghai; Phelps, Steve

doi:10.1016/j.yhbeh.2012.01.007

Cited by 138 publications

(147 citation statements)

References 81 publications

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“…21, 2017; thought to be the proximal mediators of the rewarding, empathic, and emotional aspects of social behavior, respectively 87 . Consonant with this view, insular OTR binding density correlated with reproductive success in male prairie voles 88 ; a behavioral endpoint that depends upon integration of social cues such as a partner's sexual status and situational factors with the specific behaviors under the control of the SDMN.…”

Section: Discussionmentioning

confidence: 90%

Insular Cortex Mediates Approach and Avoidance Responses to Social Affective Stimuli

Rogers

Varela

Gribbons

et al. 2017

Preprint

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Social animals detect the affective states of others and utilize this information to orchestrate appropriate social interactions. Social affective behaviors include cooperation, reproductive acts and avoiding sick individuals. In a social affective behavioral test in which experimental adult male rats were given the choice to interact with either naive or stressed conspecifics, the experimental rats demonstrated both approach and avoidant behaviors towards the conspecific, depending upon the age of the conspecific; experimental adult rats approached the stressed juvenile but avoided the stressed adult. Optogenetic inhibition of the insular cortex, a region anatomically positioned to contribute to social cognition, disrupted these behaviors. Receptors for the social nonapeptide oxytocin (OT) are found in high density within the insular cortex and here oxytocin increased intrinsic excitability and synaptic efficacy in acute insular cortex slices. Blockade of oxytocin receptors (OTRs) in the insula eliminated the effect of conspecific stress on approach behavior, while insular administration of OT recapitulated the behaviors typically observed in response to stressed conspecifics. Network analysis using Fos immunoreactivity identified functional connectivity between the insular cortex and the network of regions involved in social decision making. These results implicate insular cortex as a novel target of OT and suggest that insula is a key component in the circuit underlying age-dependent social responses to stressed conspecifics.Social animals, including humans, have an enormous repertoire of behavioral expressions that provide for the transmission of one's affective state to other members of the group 1-3 . Sensory and perceptive systems in the "social decision-making network" (SDMN) which consists of the social brain network 4 and the mesolimbic reward system 5 allow one to appraise these social stimuli and integrate them with past experiences, situational, and somatic factors to shape specific behavioral responses 6 . In addition to the SDMN, growing evidence implicates insular cortex in responding to socioemotional stimuli in humans. When tasked to identify the emotion of another from a facial expression, or to observe another suffer a painful stimulation, a reliable neural correlate is relative increase in the blood oxygen level dependent (BOLD) signal in the insular cortex 7,8 . Accordingly, emotion recognition and empathic deficits have been reported among individuals with insular cortex lesions [9][10][11][12] . Empathic processes are also disrupted in autism spectrum 1 Department of Psychology, Boston College, Chestnut Hill, MA 02467, USA 2 These authors made equal contributions to this work. *Corresponding Author: John P. Christianson, Department of Psychology, Boston College, 140 Commonwealth Avenue, Chestnut Hill, MA 02467 USA, Email: j.christianson@bc.edu, Phone: +1-617-552-3970.A note about the preprint. This manuscript was submitted to bioRxiv.org after multiple rounds of peer review. The manuscrip...

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Section: Discussionmentioning

confidence: 90%

Insular Cortex Mediates Approach and Avoidance Responses to Social Affective Stimuli

Rogers

Varela

Gribbons

et al. 2017

Preprint

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“…Specifically, these studies revealed an interaction between mating tactic (resident/wanderer) and reproductive success (sired offspring or did not), with reproductively unsuccessful wanderers having significantly more nonapeptide receptors than successful wanderers in key socio-spatial memory neural structures, in particular, RSC and SHi [35,36]. These and other results suggest socio-spatial memory is important in shaping mating tactics [24,[35][36][37]54]. In this study, differences in RSC V1aR were attributed to the presence or absence of fathers and differences in SHi OTR were shaped by the post-wean social environment.…”

Section: (B) Protective Influences Of Post-wean Environments On Sociamentioning

confidence: 98%

Perinatal and juvenile social environments interact to shape cognitive behaviour and neural phenotype in prairie voles

et al. 2015

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Social environments experienced at different developmental stages profoundly shape adult behavioural and neural phenotypes, and may have important interactive effects. We asked if social experience before and after weaning influenced adult social cognition in male prairie voles. Animals were raised either with or without fathers and then either housed singly or in sibling pairs. Males that were socially deprived before (fatherless) and after (singly housed) weaning did not demonstrate social recognition or dissociate spatial from social information. We also examined oxytocin and vasopressin receptors (OTR and V1aR) in areas of the forebrain associated with social behaviour and memory. Pre-and post-wean experience differentially altered receptor expression in several structures. Of note, OTR in the lateral septum-an area in which oxytocin inhibits social recognition-was greatest in animals that did not clearly demonstrate social recognition. The combination of absentee fathers on V1aR in the retrosplenial cortex and single housing on OTR in the septohippocampal nucleus produced a unique phenotype previously found to be associated with poor reproductive success in nature. We demonstrate that interactive effects of early life experiences throughout development have tremendous influence over brain -behaviour phenotype and can buffer potentially negative outcomes due to social deprivation.

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Section: Myodes Glareolusmentioning

confidence: 99%

“…However, the lack of evidence for the conditions that drive balancing selection on behavioral loci in natural settings creates a challenge to behavioral genetics in understanding the dynamics of behavioral loci in real-world scenarios. Genes within the arginine vasopressin-oxytocin pathway present a classic opportunity to meet this challenge; its constituent loci have been subject to extensive study because they exert major effects on animal behavior (5,11,12).The neurotransmitters vasopressin and oxytocin are evolutionarily conserved, with the vasopressin-oxytocin pathway regulating social and reproductive behaviors in many mammals including humans (5, 11, 13, 14). The behaviors associated with vasopressin and oxytocin are often mediated by the density of their receptors, notably arginine vasopressin receptor 1a (V1aR) and oxytocin receptor (OTR), in specific regions of the brain (5, 11-13).…”

mentioning

confidence: 99%

“…The behaviors associated with vasopressin and oxytocin are often mediated by the density of their receptors, notably arginine vasopressin receptor 1a (V1aR) and oxytocin receptor (OTR), in specific regions of the brain (5,(11)(12)(13). The genetic basis of the variation in V1aR density and its concomitant effect on behavior has been studied comprehensively in microtine voles (5,(15)(16)(17).…”

mentioning

confidence: 99%

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Balancing selection maintains polymorphisms at neurogenetic loci in field experiments

Lonn

Koskela

Mappes

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Most variation in behavior has a genetic basis, but the processes determining the level of diversity at behavioral loci are largely unknown for natural populations. Expression of arginine vasopressin receptor 1a (Avpr1a) and oxytocin receptor (Oxtr) in specific regions of the brain regulates diverse social and reproductive behaviors in mammals, including humans. That these genes have important fitness consequences and that natural populations contain extensive diversity at these loci implies the action of balancing selection. In Myodes glareolus, Avpr1a and Oxtr each contain a polymorphic microsatellite locus located in their 5′ regulatory region (the regulatory regionassociated microsatellite, RRAM) that likely regulates gene expression. To test the hypothesis that balancing selection maintains diversity at behavioral loci, we released artificially bred females and males with different RRAM allele lengths into field enclosures that differed in population density. The length of Avpr1a and Oxtr RRAMs was associated with reproductive success, but population density and the sex interacted to determine the optimal genotype. In general, longer Avpr1a RRAMs were more beneficial for males, and shorter RRAMs were more beneficial for females; the opposite was true for Oxtr RRAMs. Moreover, Avpr1a RRAM allele length is correlated with the reproductive success of the sexes during different phases of reproduction; for males, RRAM length correlated with the numbers of newborn offspring, but for females selection was evident on the number of weaned offspring. This report of density-dependence and sexual antagonism acting on loci within the arginine vasopressin-oxytocin pathway explains how genetic diversity at Avpr1a and Oxtr could be maintained in natural populations. Myodes glareolusM ost variation in behavior has a substantial genetic basis.Identifying loci that underpin the expression of behavior is central to our understanding of the evolution and adaptive significance of behavioral diversity (1, 2). Although many studies have found an association between genotype and behavior (2-4), few have quantified the eco-evolutionary dynamics of these genetic polymorphisms. A corollary of the diversity of behaviors exhibited in wild populations is the action of balancing selection (3, 5), a general term for mechanisms that promote fitness of alternate genotypes, including density-dependent selection (1), negative frequencydependent selection (6), heterozygote advantage (7), and sexual antagonism (8, 9). Density-and frequency-dependent selection, for example, can maintain polymorphisms at the foraging gene in laboratory populations of Drosophila melanogaster (1, 10). However, the lack of evidence for the conditions that drive balancing selection on behavioral loci in natural settings creates a challenge to behavioral genetics in understanding the dynamics of behavioral loci in real-world scenarios. Genes within the arginine vasopressin-oxytocin pathway present a classic opportunity to meet this challenge; its constituent loci have ...

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Oxytocin receptor density is associated with male mating tactics and social monogamy

Cited by 138 publications

References 81 publications

Insular Cortex Mediates Approach and Avoidance Responses to Social Affective Stimuli

Insular Cortex Mediates Approach and Avoidance Responses to Social Affective Stimuli

Perinatal and juvenile social environments interact to shape cognitive behaviour and neural phenotype in prairie voles

Balancing selection maintains polymorphisms at neurogenetic loci in field experiments

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