Valence-sensitive neurons exhibit divergent functional profiles in gregarious and asocial species

Abstract

The medial bed nucleus of the stria terminalis (BSTm) influences both social approach and social aversion, suggesting that this structure may play an important role in generating motivational and behavioral differences between gregarious and asocial species. However, no specific neurons have been identified within the BSTm that influence species-typical levels of sociality or that mediate approach and avoidance. Using five songbird species that differ selectively in their species-typical group sizes, we now demonstrate that vasotocin-immunoreactive (VT-ir) neurons of the BSTm exhibit very different immediate early gene responses to same-sex stimuli in gregarious and asocial species. Exposure to a same-sex conspecific increases VT-Fos colocalization in gregarious species while decreasing colocalization in relatively asocial species. We additionally demonstrate that these neurons are selectively activated by social stimuli that normally elicit affiliation (positively valenced social stimuli) but not by stimuli that elicit aversion (negatively valenced social stimuli). Constitutive Fos activity of the VT-ir neurons is also significantly greater in the gregarious species, and the two most social species express significantly more VT-ir neurons. These findings demonstrate that the properties of valence-sensitive neurons evolve in relation to sociality and indicate that gregarious species accentuate positive stimulus properties during social interactions.

Fig. 1.

Photomicrographs of VT-ir neurons in the BSTm of a male zebra finch at the level of the anterior commissure (A) and immediately caudal to the anterior commissure (B) (color inverted fluorescence). Asterisks indicate the location of Insets showing neurons double-labeled for VT (green) and Fos (red). (Scale bars: A, 100 μm; B, 200 μm; Insets, 50 μm.) AC, anterior commissure; BSTl, lateral bed nucleus of the stria terminalis; LS, lateral septum; MS, medial septum; PVN, paraventricular nucleus of the hypothalamus; v, ventricle.

Fig. 2.

Responses of VT neurons to a same-sex stimulus in the highly gregarious zebra finch. Percentage of VT-ir neurons in the BSTm that express Fos-ir nuclei (means ± SEM) after exposure to a same-sex conspecific or a control condition (males, solid bars; females, open bars). Two-way ANOVA (sex × condition) shows a main effect of condition (P = 0.002). Total n = 10.

Fig. 3.

Responses of VT-ir neurons to a conspecific stimulus differ between asocial and gregarious species. (A) Percentage of VT-ir neurons in the BSTm that express Fos-ir nuclei (means ± SEM) after exposure to a same-sex conspecific (filled bars) or a control condition (open bars) in two relatively asocial, territorial species [melba finch (MF) and violet-eared waxbill (VEW)], a moderately gregarious species [Angolan blue waxbill (ABW)], and a highly gregarious, colonial species [spice finch (SF)]. No sex differences were observed, and sexes are shown pooled. Two-way ANOVA (species × condition) yields a main effect of species (P = 0.01) and a species × condition interaction (P = 0.02). Different letters above the bars indicate significant species differences (P < 0.05, Fisher's protected least squares difference). Two-way ANOVA (sociality × condition) after pooling of the relatively asocial subjects (MF and VEW) and the gregarious subjects (ABW and SF) shows a main effect of sociality (P = 0.005) and a sociality × condition interaction (P = 0.01). Total n = 44. (B) Representative double-labeling for Fos (red) and VT (green) in an experimental male spice finch. DAPI nuclear stain is shown in blue. (Scale bar: 50 μm.)

Fig. 4.

Fos expression in VT-ir neurons increases in response to positively valenced social stimuli but not negatively valenced stimuli. (A) Percentage of VT-ir neurons in the BSTm that express Fos-ir nuclei (means ± SEM) in the asocial violet-eared waxbill after exposure to a control condition (open bars), a same-sex conspecific (black bars), or the subject's pairbond partner (gray bars). Different letters above the bars indicate significant group differences (Mann–Whitney tied P < 0.05, after significant Kruskal–Wallis tied P = 0.003). Total n = 16. (B) VT-Fos colocalization in control (open bars), subjugated (black bars), and nonsubjugated (gray bars) zebra finches exposed to mate competition (Kruskal–Wallis tied P = 0.03). No sex differences were observed, and sexes are shown pooled. Total n = 15.

Fig. 5.

Highly colonial species express more VT-ir neurons than do less gregarious species. Numbers of VT-ir neurons per 40-μm section (means ± SEM) in the BSTm of two relatively asocial, territorial species [melba finch (MF) and violet-eared waxbill (VEW)], a moderately gregarious species [Angolan blue waxbill (ABW)], and two highly gregarious, colonial species [spice finch (SF) and zebra finch (ZF)]. No sex differences were observed, and sexes are shown pooled. Different letters above the bars indicate significant species differences (P < 0.05, Fisher's protected least squares difference) after significant ANOVA (P < 0.0001). Total n = 96.