The neurobiology of pair bonding: Insights from a socially monogamous rodent

Department of Psychology and Program in Neuroscience, Florida State University, Tallahassee, FL 32306, USA.
Frontiers in Neuroendocrinology (Impact Factor: 7.04). 01/2011; 32(1):53-69. DOI: 10.1016/j.yfrne.2010.07.006
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The formation of enduring relationships between adult mates (i.e., pair bonds) is an integral aspect of human social behavior and has been implicated in both physical and psychological health. However, due to the inherent complexity of these bonds and the relative rarity with which they are formed in other mammalian species, we know surprisingly little about their underlying neurobiology. Over the past few decades, the prairie vole (Microtus ochrogaster) has emerged as an animal model of pair bonding. Research in this socially monogamous rodent has provided valuable insight into the neurobiological mechanisms that regulate pair bonding behaviors. Here, we review these studies and discuss the neural regulation of three behaviors inherent to pair bonding: the formation of partner preferences, the subsequent development of selective aggression toward unfamiliar conspecifics, and the bi-parental care of young. We focus on the role of vasopressin, oxytocin, and dopamine in the regulation of these behaviors, but also discuss the involvement of other neuropeptides, neurotransmitters, and hormones. These studies may not only contribute to the understanding of pair bonding in our own species, but may also offer insight into the underlying causes of social deficits noted in several mental health disorders.

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Available from: Kimberly Young, Aug 18, 2014
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    • "ted the formation of a partner preference , while an OXTA blocked this effect in females ( Cushing and Carter , 2000 ) . In addition to the role of OXT in the modulation of social behavior between pair - mates , there is abundant evidence to suggest that AVP neural circuits are crucial to pair bonding in male prairie voles ( Lim and Young , 2004 ; Young et al . , 2011 ) . Perhaps OXT and AVP receptors are differentially distributed in male and female marmosets , and this differential physiology contributes to the dissimilar behavioral patterns expressed during social interactions between pair - mates . While AVP immunereactive cells were found in several brain regions of the social behavior network ("
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    ABSTRACT: Adult male-female bonds are partly characterized by initiating and maintaining close proximity with a social partner, as well as engaging in high levels of affiliative and sociosexual behavior. Oxytocin (OXT), a neuromodulatory nonapeptide, plays a critical role in the facilitation of social bonding and prosocial behavior toward a social partner (Feldman, 2012). However, less attention has been given to whether augmentation of OXT levels in an individual alters others' perceptions and behavior toward an OXT-treated social partner. We examined social dynamics in well-established male-female pairs of marmoset monkeys (Callithrix jacchus) in which one member of the pair was administered an intranasal OXT agonist, an OXT antagonist (OXTA), or saline. OXT treatment did not alter the expression of affiliative toward an untreated partner. However, OXT did significantly influence the expression of proximity and grooming behavior with a treated partner, as a function of OXT treatment and sex. Female interest in initiating and maintaining proximity with a pair-mate was altered by OXT treatment. Untreated female marmosets departed from their saline-treated partner more frequently than they approached them, as indicated by a low proximity index score. However, when males received an intranasal OXT agonist they had a significantly increased proximity index score relative to saline, indicating that their untreated partner approached them more often than they departed from them). Saline-treated females initiated and received equivalent levels of grooming behavior. However, when female marmosets were treated with an OXT agonist their untreated partner groomed them proportionately more often, for a greater total duration, and for more time per bout, than they initiated grooming behavior. These results suggest that intranasal OXT altered male and female marmosets' stimulus properties in such a way as to increase the amount of grooming behavior that females received from their long-term mate, as well as increase female interest in initiating and maintaining proximity with their long-term mate. Furthermore, these results support the notion that central OXT activity plays an important neuromodulatory role in the maintenance of long-lasting male-female relationships.
    Frontiers in Behavioral Neuroscience 10/2015; 9. DOI:10.3389/fnbeh.2015.00251 · 3.27 Impact Factor
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    • "In a subsequent study, Young and colleagues [25] assessed partner preference in female voles in response to OT-mediated transmission in the NAcc. Female voles receiving OT infusions in the NAcc were capable of showing preference for a familiar male after only 6 h of copulationfree cohabitation; however, OT antagonist infusion blocked partner preference, even after voles were allowed to cohabitate for 24 h [24] [25]. A recent study showed that endogenous OT is released in the NAcc of the female vole during socio-sexual interactions, with fibers originating from the paraventricular and supraoptic hypothalamic neurons, well-known sites of OT synthesis [26]. "
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    ABSTRACT: Oxytocin has been previously associated with social attachment behaviours in various species, however, most studies focused on partner preference in the socially-monogamous prairie vole. In these, oxytocin treatment was shown to promote partner preference, such that females receiving either central or pulsatile peripheral administration would spend more time with a familiar male. This behavioural outcome was blocked by oxytocin receptor antagonist treatment. The aim of the current study was to further explore the preference-inducing properties of oxytocin by examining its effects on object preference on ovariectomized female rats. In other words, we assessed whether these effects would apply to objects and if they would be persistent across species. Eight rats were infused with oxytocin into the left ventricle and object preference was assessed at two delays: 30min and 4 hr. At the 30min, oxytocin-treated animals showed preference for the familiar object, whereas saline-treated controls exhibited preference for the novel object. At the 4 hr delay, both groups showed novel-object preference. Our findings suggest that oxytocin modulates object preference in the female rat at a shorter delay, similar to the findings from partner-preference studies in the prairie vole, suggesting that the mechanisms driving object preference might be in part similar to those responsible for partner preference.
    Behavioural Brain Research 08/2014; DOI:10.1016/j.bbr.2014.08.015 · 3.03 Impact Factor
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    • "To date, studies designed to answer this question have produced mixed findings [41], [42]. However, oxytocin’s effects on pro-social behavior in organisms that are evolutionarily older than humans [43] are presumably better explained by effects on affective empathy than by effects on cognitive empathy. Moreover, in humans, assessing affective empathy without the influence of cognitive empathy is difficult with self-report measures. "
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    ABSTRACT: Autism spectrum disorder is characterized by interpersonal deficits and has been associated with limited cognitive empathy, which includes perspective taking, theory of mind, and empathic accuracy (EA). The capacity for affective empathy may also be impaired. In the present study we aimed to determine if EA in normally developing individuals with varying levels of autism spectrum traits is moderated by trait affective empathy. Fifty male and fifty female participants ('perceivers') completed the Autism-Spectrum Quotient and the Balanced Emotional Empathy Scale to assess autism spectrum traits and trait affective empathy, respectively. EA was assessed using a Dutch-language version of a previously developed task and involved rating the feelings of others ('targets') verbally recounting autobiographical emotional events. Targets varied in trait emotional expressivity, assessed using the Berkeley Expressivity Questionnaire. Perceivers with more autism spectrum traits performed worse on the EA task, particularly when their trait affective empathy was relatively low. Interpersonal deficits in autism spectrum disorder may be partially explained by low cognitive empathy. Further, they might be aggravated by a limited capacity for affective empathy.
    PLoS ONE 06/2014; 9(6):e98436. DOI:10.1371/journal.pone.0098436 · 3.23 Impact Factor
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