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. 2009 Aug 11:3:15.
doi: 10.3389/neuro.08.015.2009. eCollection 2009.

Dopamine regulation of social choice in a monogamous rodent species

Brandon J Aragona  1 , Zuoxin Wang
Affiliations

Dopamine regulation of social choice in a monogamous rodent species

Brandon J Aragona et al. Front Behav Neurosci. .

Abstract

There is growing appreciation that social decision making in humans is strongly influenced by hedonic and emotional processing. The field of social neuroeconomics has shown that neural systems important for reward are associated with social choice and social preferences in humans. Here, we show that the neurobiology of social preferences in a monogamous rodent species, the prairie vole, is also regulated by neural systems involved in reward and emotional processing. Specifically, we describe how mesolimbic dopamine transmission differentially mediates the formation and maintenance of monogamous pair bonds in this species. Thus, reward processing exerts tremendous regulation over social choice behaviors that serve as the foundation of a rather complex social organization. We conclude that prairie voles are an excellent model system for the neuroscience of social choice and that complex social decision-making can be robustly explained by reward and hedonic processing.

Keywords: monogamy; nucleus accumbens; pair bond; prairie vole; social attachment; social decision making; social neuroeconomics.

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Figures

Figure 1
Figure 1
The prairie vole model. (A) Photo of an adult male prairie vole. (B) Cartoon of partner preference apparatus. Each cages is identical and food and water are available ad libitum throughout the 3-h test. (C) Male prairie voles paired with an estrogen-primed female for 24 h show a robust partner preference, i.e. spend significantly more time in side-by-side contact with their familiar mates (partners) compared to novel females that are also estrogen primed (strangers). (D) Male prairie voles paired with an ovariectomized female that is not estrogen primed for only 6 h do not show partner preferences; i.e. they display non-selective side-by-side contact. Error bars = standard error and * indicates groups are significantly different as determined by a t-test.
Figure 2
Figure 2
Dopamine regulation of pair bond formation. (A) Coronal section showing tyrosine hydroxylase immunocytochemical labeling of dorsal and ventral striatum from an adult male prairie vole. CP = caudate putamen, NAc = nucleus accumbens NAc shell, OT = olfactory tuberacle. (B) Dopamine turnover as indicated by increased concentration of the dopamine metabolite DOPAC and decreased concentration of DA from micro-dissected of NAc tissue, chemical extraction, and measurement using HPLC-ED. Male prairie voles show increased mean DA turnover 30 min after mating onset with an estrogen-primed female. (C) Blockade of DA receptors within the NAc by micro-infusion of haloperidol (Halo) prevented mating-induced partner preference formation. (D) Micro-infusion of low (0.04 ng) but not high (4.0 ng) dose of apomorphine (Apo) induced partner preferences in the absence of mating.
Figure 3
Figure 3
Opposing regulation of pair bond formation by D2- and D1-like dopamine signaling systems within the NAc shell. (A) Activation of D2-like receptors within the NAc shell by micro-infusion of the D2-specific agonist quinpirole (D2 ago) induced partner preferences in the absence of mating. Activation of D1-like receptors within the shell using the D1-specific agonist SKF 38393 (D1 ago) failed to induced partner preference formation and prevented quinpirole-induced partner preferences. (B) Activation of D1-like receptors also prevented partner preferences induced by mating. (C) Decreased activation of protein kinase A (PKA) using Rp-cAMPS (PKA ↓) induced partner preferences in the absence of mating, whereas activation of PKA using Sp-cAMPS (PKA ↑) did not. (D) While decreased activation of PKA using Rp-cAMPS (PKA ↓) did not interfere with mating-induced partner preference formation, activation of PKA using Sp-cAMPS (PKA ↑) interfered with this behavior.
Figure 4
Figure 4
Up-regulation of D1-like receptors within the NAc of pair bonded animals. (A) Representative examples of D1-like receptor binding within the dorsal and ventral striatum of sexually naive adult male prairie voles (left) and pair bonded males (paired with a female for 2 weeks; right). (B) Representative examples for D2-like receptor binding. (C) Quantification of receptor binding expressed as percent of control subjects. Pair bonded males show a significant increase in D1-like receptor binding within the NAc but not the CP (caudate-putamen). There is no significant change in D2-like receptor binding within either striatal region.
Figure 5
Figure 5
Dopamine regulation of pair bond maintenance as indicated by selective aggression toward novel females. (A) Photo of pair bonded mates engaged in affiliative behavior (typically huddling or side-by-side contact). (B) Pair bonded male (right) showing aggressive behavior toward an unfamiliar/novel female (stranger; left). (C) Quantification of affiliative behavior during a 6-min resident intruder test of selective aggression. Pair bonded males show significantly more affiliative behavior than other group when presented with their familiar partner, but significantly less affiliation when presented with unfamiliar females (strangers). Blockade of either D1- or D2-like receptors restores affiliative behavior in pair bonded males to levels expressed by sexually naive males being exposed to a female for the first time. (D) While sexually naive (presented with a female) and pair bonded males (presented with their partners) show no aggressive behavior, pair bonded males show significantly greater levels of aggression when presented with a novel female (stranger). Selective aggression is blocked by D1-like (but not D2-like) receptors within the NAc.
Figure 6
Figure 6
Differential regulation of pair bond formation and maintenance by dopamine transmission within the NAc. (A) Cartoon based on (Arbuthnott and Wickens, 2007) showing the portion of the NAc shell where DA manipulations effect pair bond formation. (B) Diagram of D2-like signaling pathway involved in partner preference formation. (C) Diagram of D1-like signaling pathway that prevents partner preference formation. (D) Cartoon of medium spiny neuron (MSN) within the NAc receive glutamate projections to the heads of spines and dopaminergic projections to the neck of spines. This diagram represents D1-like receptor expression in sexually naive males. (E) A cartoon depicting the up-regulation of D1-like receptors in pair bonded male prairie voles.
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