Variation in Oxytocin Receptor Density in the Nucleus Accumbens Has Differential Effects on Affiliative Behaviors in Monogamous and Polygamous Voles

Center for Behavioral Neuroscience, School of Medicine, Emory University, Atlanta, Georgia 30033, USA.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 03/2009; 29(5):1312-8. DOI: 10.1523/JNEUROSCI.5039-08.2009
Source: PubMed


Oxytocin receptors in the nucleus accumbens have been implicated in the regulation of alloparental behavior and pair bond formation in the socially monogamous prairie vole. Oxytocin receptor density in the nucleus accumbens is positively correlated with alloparenting in juvenile and adult female prairie voles, and oxytocin receptor antagonist infused into the nucleus accumbens blocks this behavior. Furthermore, prairie voles have higher densities of oxytocin receptors in the accumbens than nonmonogamous rodent species, and blocking accumbal oxytocin receptors prevents mating-induced partner preference formation. Here we used adeno-associated viral vector gene transfer to examine the functional relationship between accumbal oxytocin receptor density and social behavior in prairie and meadow voles. Adult female prairie voles that overexpress oxytocin receptor in the nucleus accumbens displayed accelerated partner preference formation after cohabitation with a male, but did not display enhanced alloparental behavior. However, partner preference was not facilitated in nonmonogamous meadow voles by introducing oxytocin receptor into the nucleus accumbens. These data confirm a role for oxytocin receptor in the accumbens in the regulation of partner preferences in female prairie voles, and suggest that oxytocin receptor expression in the accumbens is not sufficient to promote partner preferences in nonmonogamous species. These data are the first to demonstrate a direct relationship between oxytocin receptor density in the nucleus accumbens and variation in social attachment behaviors. Thus, individual variation in oxytocin receptor expression in the striatum may contribute to natural diversity in social behaviors.

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Available from: Sara M. Freeman, Apr 03, 2014
    • "Site-specific delivery of oxytocin antagonists into the nucleus accumbens decreases alloparental behaviors in this species, demonstrating that OTR binding is important for the display of the behavior and not simply a product of it (Olazabal and Young, 2006b). Increasing the number of receptors in the nucleus accumbens also accelerates the establishment of a sexual partner preference in female prairie voles (Ross et al., 2009). In meadow voles, OTR density in the central amygdala and social behavior vary seasonally with day length, and OTR density in the lateral septum is negatively correlated with same-sex affiliative behavior in females (Beery and Zucker, 2010; Beery et al., 2014). "
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    ABSTRACT: Naturally occurring variations in neuropeptide receptor distributions in the brain contribute to numerous mammalian social behaviors. In naked mole-rats, which live in large social groups and exhibit remarkable reproductive skew, colony-related social behaviors vary with reproductive status. Here we examined whether variation in social status is associated with variations in the location and/or density of oxytocin binding in this species. Autoradiography was performed to assess forebrain oxytocin receptor (OTR)density in breeding and non-breeding naked mole-rats of both sexes. Overall, males exhibited higher OTR binding in the medial amygdala in comparison to females. While there were no main effects of reproductive status in any region, a sex difference in OTR binding in the nucleus accumbens was mediated by status. Specifically, breeding males tended to have more OTR binding than breeding females in the nucleus accumbens, while no sex difference was observed in subordinates. These effects suggest that oxytocin may act in a sex- and region-specific way that corresponds to reproductive status and associated social behaviors. Copyright © 2015 IBRO. Published by Elsevier Ltd. All rights reserved.
    No preview · Article · Jul 2015 · Neuroscience
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    • "Oxytocin (OT) and vasopressin (AVP) were early targets of this research, as these neuropeptides were known to modulate speciesspecific social behaviors such as sexual behavior, aggression, maternal care, and olfaction related to conspecific identification [6] [7] [8] [9] [10] [11] [12]. Neuroanatomical studies have revealed that, although there are minor species differences in cell bodies and fibers, there are dramatic differences in regional receptor distribution between monogamous and promiscuous vole species [13] [14] [15]. Specifically, monogamous prairie voles have higher densities of the vasopressin A1 receptor (V1aR), in the BNST, ventral pallidum (VP), central amygdala (CeA), basolateral amygdala (BLA), and accessory olfactory bulbs (AOB) than promiscuous montane voles [16] [17] [18]. "
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    ABSTRACT: We have shown previously that female rats given their first copulatory experiences with the same male rat display mate guarding behavior in the presence of that male provided a female competitor is also present. Females given access to the familiar male show more Fos induction within regions of the brain that contain oxytocin (OT) and vasopressin (AVP) cell bodies, notably the supraoptic (SON) and paraventricular nuclei (PVN) relative to females given sexual experience with different males. The present experiments examined whether the Fos induction we previously observed within the SON and PVN occurred within OT and/or AVP neurons, and whether exogenous administration of OT or AVP prior to female rats first sexual experience could potentiate the acquisition of mate guarding behavior. Female rats that display conditioned mate guarding had significantly more double-labeled Fos/OT neurons in both SON and PVN, and significantly more Fos/AVP neurons in the PVN. Peripheral administration of OT or AVP prior to their first sexual experience with the familiar male facilitated different aspects of mate guarding: OT augmented affiliative behaviors and presenting responses whereas AVP augmented interference behavior. These results indicate that female rats' first experiences with sexual reward when paired with the same male induce changes to bonding networks in the brain. Moreover peripheral administration of OT or AVP during their first sexual experience can augment different aspects of mate guarding behavior. Copyright © 2015. Published by Elsevier Inc.
    Full-text · Article · Feb 2015 · Physiology & Behavior
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    • "Keebaugh and Young (2011) found that viral vector infusions that increased OXTR in the NA of weanling females facilitated adult spontaneous maternal behavior in prairie voles. Overexpression of NA OXTR in adult females was not effective (Ross et al., 2009), suggesting that the presence of OXTR during development was important (Keebaugh and Young, 2011). However, according to these authors, the presence of OXTR during development was not Fig. 1. "
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    ABSTRACT: Parental behavior is commonly displayed by progenitors. However, other individuals, genetically related (e.g. siblings, aunts, uncles) or not with the newborns, also display parental behavior (commonly called alloparental, or adoptive behavior). I hypothesize that species that live in family or social groups where other non-reproductive members (males and females) take care of infants, have brain adaptations to promote or facilitate that behavioral response. The present work revises the evidence supporting the hypothesis that high density of oxytocin receptors (OXTR) in the nucleus accumbens (NA) is one of those adaptations. All species known to have high NA OXTR show not only female, but also male alloparental care. Therefore, I predict that high NA OXTR could be present in all species in which juvenile and adult male alloparental behavior have been observed. Strategies to test this and other alternative working hypothesis and its predictions are presented.
    Full-text · Article · Oct 2014 · Journal of Physiology-Paris
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