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Review
. 2016 Jun:38:80-8.
doi: 10.1016/j.conb.2016.04.011. Epub 2016 Apr 30.

The ties that bond: neurochemistry of attachment in voles

Kyle Gobrogge  1 , Zuoxin Wang  2
Affiliations
Review

The ties that bond: neurochemistry of attachment in voles

Kyle Gobrogge et al. Curr Opin Neurobiol. 2016 Jun.

Abstract

In socially monogamous prairie voles (Microtus ochrogaster), mating induces three primary types of behavior; namely, partner preference, selective aggression toward conspecific strangers, and bi-parental care, making this rodent an ideal model system to study sociality and underlying neurochemical mechanisms associated with monogamous mating strategies. Here, we highlight species differences in neurochemical receptor distributions associated with mating experience leading to the establishment of stable pair-bonds. Specifically, we illustrate the role of nucleus accumbens dopamine in programming the formation and maintenance of monogamous bonds and describe the role of anterior hypothalamic vasopressin in the regulation of selective aggression. We conclude by discussing recent molecular work in voles and emphasize the importance of this rodent for future research in the behavioral neurobiology field.

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Figures

Figure 1
Figure 1. Laboratory characterization of mating-induced pair-bonding behavior
(a) Photo depicts a pair-bonded male and female prairie vole displaying side-by-side (cuddling) contact (Photo by C. Badland & A. Smith). (b) In male and female prairie voles, 6 hrs of social cohabitation, without mating, is not sufficient to induce partner preference, as voles spend approximately an equal amount of contact time with their partner or with a stranger. Conversely, 24 hrs of cohabitation with successful copulation promotes partner preference formation, as voles spend significantly more time in side-by-side contact with their partner than with an unfamiliar stranger during a 3 hr partner preference assay. (c) Photo shows a pair-bonded male prairie vole (top) preparing to attack an unfamiliar stranger male prairie vole (bottom; Photo by C. Badland & A. Smith). (d) Sexually inexperienced (Naïve) male prairie voles do not display aggressive behavior toward a stranger, although successful mating and two weeks of social cohabitation engenders escalated selective aggression toward stranger male and female conspecifics but not toward familiar female partners. (e) Photo illustrates a pair-bonded male and female prairie vole huddling over and protecting their newly born pups (Photo by C. Badland & A. Smith). (f) Male and female prairie vole parents spend equivalent time in their natal nest huddling, contacting, and licking/grooming their offspring. Bars indicate means �� standard error of the mean. Bars with different Greek letters differ significantly from each other. *: p < 0.05. Adapted from [2,32•,40,61].
Figure 2
Figure 2. Microtine species differences in neurotransmitter receptor distribution and social behavior
Prairie voles display a socially monogamous life strategy after mating and pair-bonding (Left Image) while Meadow and Montane voles’ exhibit socially promiscuous behavior (Right Image). Vasopressin V1a-type receptor (V1aR) expression in the ventral pallidum (VP) and oxytocin receptor (OTR) density in the medial prefrontal cortex (mPFC), nucleus accumbens (NAcc), and bed nucleus of the stria terminalis (BNST) are both higher in sexually naïve prairie voles (Left) while promiscuous voles have fewer endogenous V1a/OT receptors available in these brain regions (Right). Species differences in neuropeptide receptor density have been shown to explain why these systems may be involved in the evolution of divergent mating strategies in across rodent species. Conversely, dopamine D1 receptor (D1R) expression is higher in the NAcc of non-monogamous voles (Right) and lower in prairie voles (Left). Species differences in dopamine neurotransmitter receptor density have been shown to explain why prairie voles display mating-induced selective aggression while meadow voles exhibit general levels of aggressive behavior toward conspecific animals. (Illustration by C. Badland). Adapted from [19,21•,22,26,28••,29•,62-64].
Figure 3
Figure 3. Pair-bonding-induced neuromodulator receptor plasticity and sociality in the prairie vole
Sexually naïve male prairie voles (Left) and pair-bonded male prairie voles (Right) exhibit experience-dependent changes in neurotransmitter receptor density in select brain regions including the anterior hypothalamus (AH) and nucleus accumbens (NAcc). Specifically, successful mating and pair-bonding site-specifically enhances the density of vasopressin V1a-type receptor (V1aR) expression in the AH and oxytocin receptor (OTR) and dopamine D1-type receptor (D1R) density in the NAcc. These mating-induced neuroplastic changes in receptor densities explain the behavioral switch from general patterns of social affiliation and aggression to robust social memory and selective aggression in pair-bonded male prairie voles. (Illustration by C. Badland). Adapted from [28••,32•,34••,64].
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References

    1. Young LJ, Wang Z. The neurobiology of pair bonding. Nat Neurosci. 2004;7:1048–1054. - PubMed
    1. Young KA, Gobrogge KL, Liu Y, Wang Z. The neurobiology of pair bonding: insights from a socially monogamous rodent. Front Neuroendocrinol. 2011;32:53–69. - PMC - PubMed
    1. Insel TR, Preston S, Winslow JT. Mating in the monogamous male: behavioral consequences. Physiol Behav. 1995;57:615–627. - PubMed
    1. Coccaro EF, Kavoussi RJ, Hauger RL, Cooper TB, Ferris CF. Cerebrospinal fluid vasopressin levels: correlates with aggression and serotonin function in personality-disordered subjects. Arch Gen Psychiatry. 1998;55:708–714. - PubMed
    1. Ditzen B, Schaer M, Gabriel B, Bodenmann G, Ehlert U, Heinrichs M. Intranasal oxytocin increases positive communication and reduces cortisol levels during couple conflict. Biol Psychiatry. 2009;65:728–731. - PubMed

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