Behavioral effects of hindbrain vasotocin in goldfish are seasonally variable but not sexually dimorphic

Abstract

We have previously demonstrated that centrally administered vasotocin (VT) inhibits social approach toward same-sex conspecifics in male and female goldfish, and that this behavioral effect is dependent upon VT projections to the hindbrain. We now show that there are no sex differences in sensitivity to the behavioral effects of VT, though differences do exist in responsiveness across seasons in both sexes. A central dose of 1 microg, but not 200 ng, inhibited social approach in goldfish in non-reproductive condition, whereas a dose as low as 40 ng inhibited social approach in fish in full reproductive condition. In males and females in full reproductive condition, social approach behavior was facilitated by central administration of 500 ng of a V(1A) specific antagonist. In addition, the behavioral effects of exogenously administered central VT were blocked by central administration of 1 microg of a V(1A) antagonist. These results demonstrate that the propensity to approach a conspecific, a simple behavior underlying many social interactions, is controlled by a V(1A)-like receptor, and that VT's behavioral effects depend on reproductive context. Quantitative real-time PCR showed that the seasonal changes in behavioral responsiveness to VT are associated with changes in the expression of a V(1A)-like receptor in the hindbrain, but not the mid- or forebrain, indicating that the seasonal regulation of social approach behavior likely depends on the local modulation of the expression of this receptor within a primitive peptide circuit in this species.

Fig. 1

Mean (±SEM) time spent in proximity to a conspecific stimulus after ICV administration of saline (open bars) or VT at 3 doses (solid bars; 200 ng, 40 ng, 5 ng) for male goldfish (A) and female goldfish (B) in full reproductive condition. *p < 0.05.

Fig. 2

Mean (±SEM) time spent in proximity to a conspecific stimulus after ICV administration of saline (open bars) or VT at 2 doses (solid bars; 1 µg, 200 ng) for male goldfish (A) and female goldfish (B) in late fall non-reproductive condition. *p < 0.05.

Fig. 3

(A) Mean (±SEM) time spent in proximity to a conspecific stimulus after ICV administration of saline followed by saline (open bar), saline followed by 40 ng VT (solid bars), or 500 ng of the V_1A specific antagonist followed by 40 ng VT (checkered bar) in female goldfish in full reproductive condition. (B) Mean (±SEM) time spent in proximity to a conspecific stimulus after ICV administration of saline (open bars) or 500 ng of the V_1A specific antagonist (checkered bars) for both male and female fish in full reproductive condition. *p < 0.05.

Fig. 4

The nucleotide sequence of the goldfish vasotocin receptor mRNA transcript. The beginning and end of the open reading frame are highlighted and the region amplified by qPCR is underlined in italics.

Fig. 5

Alignment of the goldfish canonical VTR open reading frame (nucleotides 249–1445) with VTR/V_1AR amino acid sequences for the white sucker (Catostomus commersoni), pufferfish (Takifugu rubripes), rat (Rattus norvegicus), and human (Homo sapiens). Shaded areas indicate conserved amino acid residues. Dots indicate conserved residues in vasopressin family receptors that may be involved in nonapeptide recognition (Mahlmann et al., 1994; Sharif and Hanley, 1992). The seven putative hydrophobic transmembrane domains are boxed. Solid line above sequence denotes C terminus repeated motifs in the white sucker sequence (Mahlmann et al., 1994).

Fig. 6

Logarithmic plots of the qPCR amplification results for hindbrain samples (A) and mid-/forebrain samples (B). There was a strong trend for higher VTR expression in hindbrain samples from fish killed during the reproductive season than from fish killed outside of the reproductive season, as evidenced by higher 1/Ct scores (C; p = 0.06). No similar trend was observed in the mid-/forebrain samples.