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Differential signaling through certain dopamine receptors promotes selective aggression towards strangers in the characteristically monogamous prairie voles.

Monogamy is rare among mammals, but the binding mechanisms in species that form lasting bonds with their mates might have parallels in reward learning and addiction. Indeed, previous studies have shown that dopamine signalling in the nucleus accumbens (NAc), part of the mesolimbic reward system, is required for pair-bond formation in prairie voles, which are characteristically monogamous. A new study in Nature Neuroscience reports that differential signalling through certain dopamine receptors is also important for the maintenance of pair bonds by promoting selective aggression towards strangers.


Image courtesy of B. J. Aragona, Florida State University, USA.

After 24 h of cohabitation and mating with a female, sexually naive male prairie voles come to prefer the contact of their mating partner to that of a novel female. This partner preference requires signalling through D2-like dopamine receptors in the NAc, and Aragona et al. show that this signalling specifically occurs in the rostral shell of the NAc, a region that is associated with appetitive conditioning in other animals. By contrast, a D1-like receptor agonist infused into the NAc blocked mating-induced partner preference, indicating differential effects of dopaminergic signalling through these two types of receptor.

Partner preference is an initial prerequisite for lasting pair-bond formation, but complete transition to a pair bond also requires that stranger conspecifics, including potential new mates, be actively rejected. Given the opposing actions of D1- and D2-like receptors in partner preference formation, Aragona and co-workers asked whether dopaminergic signalling in the NAc was also important for the development of selective aggression towards novel females. They found that fully pair-bonded male prairie voles had higher levels of D1-like receptors in the rostral core and shell of the NAc compared with naive males. Furthermore, blocking these receptors with a D1-like receptor antagonist blocked aggressive behaviour towards novel females.

The authors therefore suggest that a reorganization of dopaminergic signalling in the NAc contributes to the transition from an affiliative approach towards novel females observed in naive males to selective aggression in bonded males, a behaviour that helps to maintain an established partnership. Interestingly, similar opposing regulation by D1 and D2-like receptors also occurs in drug-seeking behaviour.

The monogamous pair bonds of prairie voles are unusual, even among vole species. Meadow voles are less social overall and have more promiscuous mating habits, and Aragona and colleagues show that male meadow voles have higher basal levels of D1-like receptors in the NAc. Blocking D1-like receptors increased affiliative behaviour in these voles, consistent with a role for this species difference in determining their naturally asocial ways, and a more general role for dopaminergic signalling in the organization of social behaviour.

Cara Allen

References

Aragona, B. J. et al. Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds. Nature Neurosci. 9, 133–139 (2006) | Article | PubMed |