Social contact elicits immediate-early gene expression in dopaminergic cells of the male prairie vole extended olfactory amygdala

Abstract

Male prairie voles (Microtus ochrogaster) are a valuable model in which to study the neurobiology of sociality because, unlike most mammals, they pair bond after mating and display paternal behaviors. Research on the regulation of these social behaviors has highlighted dopamine (DA) neurotransmission in both pair bonding and parenting. We recently described large numbers of dopaminergic cells in the male prairie vole principal nucleus of the bed nucleus of the stria terminalis (pBST) and posterodorsal medial amygdala (MeApd), but such cells were very few in number or absent in the non-monogamous species we examined, including meadow voles. This suggests that DA cells in these sites may be important for sociosexual behaviors in male prairie voles. To gain some insight into the function of these DAergic neurons in male prairie voles, we examined expression of the immediate-early genes (IEGs) Fos and Egr-1 in tyrosine hydroxylase (TH)-immunoreactive (TH-ir) cells of the pBST and MeApd after males interacted or not with one of several social stimuli. We found that IEGs were constitutively expressed in some TH-ir neurons under any social condition, but that IEG expression in these cells decreased after a 3.5-h social isolation. Thirty-minute mating bouts (but not 6- or 24-h bouts) that included ejaculation elicited greater IEG expression in TH-ir cells than did non-ejaculatory mating, interactions with a familiar female sibling, or interactions with pups. Furthermore, Fos expression in TH-ir cells was positively correlated with the display of copulatory, but not parental, behaviors. These effects of mating were not found in other DA-rich sites of the forebrain (including the anteroventral periventricular preoptic area, periventricular anterior hypothalamus, zona incerta, and arcuate nucleus). Thus, activity in DAergic cells of the male prairie vole pBST and MeApd is influenced by their social environment, and may be particularly involved in mating and its consequences, including pair bonding.

Figure 1

Number of Fos-ir cells (Mean ± SEM) in four sections through the pBST and seven sections through the MeApd after male prairie voles interacted with one of several stimuli for 30 min. Bars with any of the same letters above them do not significantly differ from each other.

Figure 2

Percentage of TH-ir cells expressing Fos (Mean ± SEM) in the pBST and MeApd after male prairie voles interacted with one of several stimuli for 30 min. Bars with any of the same letters above them do not significantly differ from each other.

Figure 3

Photomicrographs of the pBST (top row) and MeApd (bottom row) from representative males in the ALONE, NON EJAC, and EJAC groups in Experiment Ia. Small arrows in top left panel indicate cells that are single-labeled with TH immunoreactivity (blue cytoplasmic label). Large arrows in top middle panel indicate cells that are single-labeled with Fos immunoreactivity (brown nuclear label). Dual-labeled cells are highlighted at higher magnification in the two panels showing EJAC males. Scale bar in bottom left panel = 50 μm. Scale bar in bottom right panel inset = 10 μm.

Figure 4

Correlations between the percentage of TH-ir cells in the pBST (left) and MeApd (right) that also contained Fos immunoreactivity and the duration of time spent mounting and thrusting by EJAC males (squares) and NON EJAC males (circles) during a 30-min test with a sexually receptive female. Time engaged in male sexual behavior (bottom row) is the summed duration of mounting, thrusting, and ejaculating. See Table 3 for correlations between other behaviors and the percentage of TH-ir cells that also contained Fos immunoreactivity.

Figure 5

Number of Egr-1-ir cells (Mean ± SEM) in two sections of the pBST and three sections through the MeApd after male prairie voles interacted with one of several stimuli for 30 min. Bars with any of the same letters above them do not significantly differ from each other.

Figure 6

Percentage of TH-ir cells (Mean ± SEM) in the pBST and MeApd that also contained Egr-1 immunoreactivity after male prairie voles interacted with one of several stimuli for 30 min. Bars with any of the same letters above them do not significantly differ from each other.

Figure 7

Number of Fos-ir cells (Mean ± SEM) in four sections through the pBST and seven sections through the MeApd after male prairie voles mated, interacted with a familiar female sibling, or remained alone for 6 or 24 h. Note that the Y-axis scales for both sites are the same as that in Figure 1. Bars with any of the same letters above them do not significantly differ from each other.

Figure 8

Percentage of TH-ir cells also containing Fos immunoreactivity (Mean ± SEM) in the pBST and MeApd after male prairie voles mated, interacted with a familiar female sibling, or remained alone for 6 or 24 h. Note that the Y-axis scales for both sites are the same as that in Figure 2. Bars with any of the same letters above them do not significantly differ from each other.