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First published online April 18, 2006
Journal of Experimental Biology 209, v-a (2006)
Copyright © 2006 The Company of Biologists Limited
doi: 10.1242/jeb.02221
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Outside JEB

FIRST AND ONLY LOVE

Susan Sangha

Westfaelische Wilhelms Universitaet Muenster

sangha{at}uni-muenster.de


Figure 1

Monogamy is defined as the condition of having only one mate. But have you ever wondered what's happening at the neuronal level when we choose that special someone? In a recent paper in Nature Neuroscience, Brandon Aragona and colleagues show that dopamine activity in the nucleus accumbens, a structure in the brain known to be involved in controlling social interactions, is necessary for pair bonding behaviour in the monogamous prairie vole.

The neurobiology underlying both pair bond formation and maintenance is poorly understood. However, the prairie vole has proven to be an excellent model for addressing these questions because they easily form pair bonds and the behaviour they emit upon forming a pair bond is readily quantifiable. A pair bond is established when a male vole prefers a particular mating partner and potential female mates are subsequently rejected aggressively. It is known that dopamine transmission in the nucleus accumbens via the D2-like receptors (D2 receptors) and D1-like receptors (D1 receptors) mediates both approach and avoidance behaviours and thus the authors focused on this system to study pair bond formation and maintenance.

The team measured partner preference in a male prairie vole by recording the duration of side-by-side contact it made with a particular female and when it displayed selective aggression by the number of attacks and aggressive postures the male vole struck toward other female voles. Activation of the D2-like receptors, but not D1-like receptors, in the nucleus accumbens had previously been shown to be important in forming a pair bond. However, it was unclear where in the nucleus accumbens this signaling occurs, or, how a pair bond is maintained. By injecting a D2 receptor agonist into specific subregions of the nucleus accumbens, the authors demonstrated that dopamine activity via the D2 receptors in the rostral shell of the nucleus accumbens is necessary to form a pair bond.

Knowing that a long-lasting change in behaviour is associated with changes in synaptic connectivity, the authors hypothesized that a reorganization of the dopamine signaling system in the nucleus accumbens was responsible for pair bond maintenance and found an increase in D1 receptors in the nucleus accumbens 2 weeks after forming a partner preference, which was associated with increased aggression toward other females. Since dopamine activity via the D1 receptors blocks pair bond formation, the authors hypothesized that the upregulation of these receptors prevents the formation of a second pair bond, thus promoting stable maintenance of the initial pair bond.

This study clearly demonstrates that dopamine activity in the nucleus accumbens regulates monogamous pair bonding. Initially, in a sexually naive male, dopaminergic signaling, primarily via D2 receptors, facilitates a partner preference, a positive association. Subsequent to forming a pair bond, dopaminergic signaling, now primarily via D1 receptors, indicates an aversive stimulus thus increasing aggression towards other females and preventing a second pair bond. Dopamine signaling in the nucleus accumbens is not only important for pair bonding but also in drug addiction. Thus, the data here also supports the hypothesis that drugs of abuse target neural systems that evolved to mediate adaptive behaviours such as social bonding.

References

Aragona, B. J., Liu, Y., Yu, Y. J., Curtis, J. T., Detwiler, J. M., Insel, T. R. and Wang, Z. (2006). Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds. Nature Neurosci. 9, 133-139.[CrossRef][Medline]





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