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
Source: PubMed


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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    • "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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    • "All of the studies described above examined polygamous laboratory rodents, but it would be interesting to study the relationships among the hypothalamic OX system and social interactions, sex, and reproductive experience in a monogamous rodent such as the prairie vole (Microtus ochrogaster). Male and female prairie voles share more aspects of their behavioral repertoires when compared to most polygamous rodents, with both sexes of prairie vole forming lifelong pairbonds after mating and later contributing parental care to their offspring [11] [76]. Furthermore, reproductive experience and pairbonding alter anxiety-related behavior [32,37,39] and energy balance [10] in male prairie voles in ways that are more typically found in postpartum female mammals [see 40, 74]. "
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    ABSTRACT: Large populations of cells synthesizing the neuropeptide orexin (OX) exist in the caudal hypothalamus of all species examined and are implicated in physiological and behavioral processes including arousal, stress, anxiety and depression, reproduction, and goal-directed behaviors. Hypothalamic OX expression is sexually dimorphic in different directions in laboratory rats (F>M) and mice (M>F), suggesting different roles in male and female physiology and behavior that are species-specific. We here examined if the number of hypothalamic cells immunoreactive for orexin A (OXA) differs between male and female prairie voles (Microtus ochrogaster), a socially monogamous species that pairbonds after mating and both sexes care for offspring, and if reproductive experience influences their number of OXA-immunoreactive (OXA-ir) cells. The total number of OXA-ir cells did not differ between sexes, but females had more OXA-ir cells than males in anterior levels of the caudal hypothalamus, while males had more OXA-ir cells posteriorly. Sexually experienced females sacrificed 12 days after the birth of their first litter, or one day after birth of a second litter, had more OXA-ir cells in anterior levels but not posterior levels of the caudal hypothalamus compared to females housed with a brother (incest avoidance prevents sibling mating). Male prairie voles showed no effect of reproductive experience but showed an unexpected effect of cohabitation duration regardless of mating. The sex difference in distribution of OXA-ir cells, and their increased number in anterior levels of the caudal hypothalamus of reproductively experienced female prairie voles, may reflect a sex-specific mechanism involved in pairbonding, parenting, or lactation.
    Peptides 05/2014; 57. DOI:10.1016/j.peptides.2014.05.004 · 2.62 Impact Factor
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