A critical role for nucleus accumbens dopamine in partner-preference formation in male prairie voles

Abstract

Although the role of nucleus accumbens (NAcc) dopamine (DA) in reward learning has been extensively studied, few investigations have addressed its involvement in learning socially relevant information. Here, we have examined the involvement of NAcc DA in social attachment of the "monogamous" prairie vole (Microtus orchrogaster). We first demonstrated that DA is necessary for the formation of social attachment in male prairie voles, because administration of haloperidol blocked, whereas apomorphine induced, partner-preference formation. We then provided the first descriptions of DA neuroanatomy and tissue content in vole NAcc, and mating appeared to induce a 33% increase in DA turnover. We also showed that administration of haloperidol directly into the NAcc blocked partner preferences induced by mating and apomorphine. In addition, administration of apomorphine into the NAcc but not the caudate putamen induced partner preferences in the absence of mating. Together, our data support the hypothesis that NAcc DA is critical for pair-bond formation in male prairie voles.

Fig. 1.

Peripheral administration of dopamine drugs influenced partner preferences in male prairie voles. A, Males injected intraperitoneally with saline and mated with a partner for 24 hr had more side-by-side contact with the partner versus a conspecific stranger. This partner preference was not seen in males receiving saline injections containing the dopamine antagonist Halo. B, Males injected with saline and paired with a partner for 6 hr in the absence of mating showed nonselective side-by-side contact during the partner-preference test. However, males receiving the low (0.5 μg) but not the high (5 and 50 μg) dose of the dopamine agonist Apo had more contact with the partner versus a stranger. *p < 0.05; paired samplest test. Error bars indicate SEM.

Fig. 2.

A–D, Photomicrographs displaying immunoreactive staining for TH (left) and DAT (right) at rostral (A, B) and caudal (C,D) levels of NAcc from representative brain sections of male prairie voles. ac, Anterior commissure. Scale bar, 500 μm.

Fig. 3.

Effect of mating on dopamine turnover and neurochemical content in the male prairie vole brain. A, Schematic illustration of tissue-punch location for NAcc and CP. The illustration is from the atlas of Paxinos and Watson (1986), plate 11.B, Mean dopamine turnover from the NAcc, CP, and PVN for male prairie voles paired with same-sex siblings (white bars), a novel female (gray bars), or a novel female with mating (black bars). Mated males showed a 33% increase in dopamine turnover in the NAcc compared with control and nonmated males; however, this difference was not statistically significant. A similar pattern of increase is seen in the CP but not the PVN. Error bars indicate SEM. C, Table showing mean content (picograms per microgram of protein ± SEM) of DA, DOPAC, HVA, NE, 5-HT, and 5-HIAA in the NAcc.

Fig. 4.

NAcc dopamine is involved in partner-preference formation of male prairie voles. A, Males microinjected with artificial CSF into the NAcc and mated with a partner for 24 hr had more side-by-side contact with the partner versus a conspecific stranger. This mating-induced partner preference was blocked by NAcc administration of CSF containing Halo. B, Males microinjected with CSF and paired with a partner for 6 hr in the absence of mating showed nonselective side-by-side contact with the partner or stranger. However, males receiving the low (0.04 ng) but not the high (4 ng) dose of the dopamine agonist Apo displayed partner preferences. This apomorphine-induced (0.04 ng) partner preference was blocked by coadministration of haloperidol (0.4 ng). In addition, apomorphine (0.04 ng) failed to induce partner preferences when administered into the CP. *p < 0.05 and **p < 0.005; paired samples t test. Error bars indicate SEM.

Fig. 5.

A schematic illustration (left) showing locations of microinjections of apomorphine into the NAcc or CP, and a representative photomicrograph of vole brain section (right) displaying the site of microinjection into the NAcc.