A primitive social circuit: vasotocin–substance P interactions modulate social behavior through a peripheral feedback mechanism in goldfish

Abstract

At its core, the polyvagal theory proposes that peptides affect simple social behaviors through influences on hindbrain autonomic processes. To test this mechanism, we compared the effects of fore- and hindbrain infusions of vasotocin (VT) on social approach behavior in goldfish. VT infusions into the 4th ventricle, which ink infusions verified did not move rostrally to the forebrain, inhibited social approach at a lower dose than did infusions into the 3rd ventricle, which did diffuse to the hindbrain. Thus, VT actions in the hindbrain appear to modulate this simple social behavior. We then identified a population of substance P (SP)-immunoreactive cells in the hindbrain that are encapsulated by putative VT terminals, and determined that those cells project to the periphery. Injecting SP peripherally, as with infusing VT centrally, inhibited social approach, and peripheral injections of an SP antagonist, but not central infusions, abolished the behavioral effects of central VT infusions. We therefore propose that VT inhibits social approach by activating SP cells in the hindbrain, which then induce changes in body state that feed back to the brain. Central VT infusions did not inhibit feeding, suggesting that this VT mechanism selectively affects appetitive social responses. Because VT projections to the hindbrain are highly conserved in vertebrates, influences on peripheral feedback processes like the one we have described in goldfish may reflect how VT affected simple social behaviors in ancestral vertebrates and thus preadapted members of this peptide family to play increasingly complex roles in social and emotional regulation in modern animals.

Nonapeptide influences on social behaviour: effects of vasotocin and isotocin on shoaling and interaction in zebrafish

“…We saw a marked reduction in social interaction in fish that received AVT, mirroring findings in goldfish in which AVT inhibited social approach (Thompson & Walton, 2004;Thompson et al, 2008). This effect of AVT on social interaction also has parallels in the findings of Filby et al (2010) who showed that AVT reduced aggressive behaviours, including chasing of conspecifics, in small groups of zebrafish.…”

Vasotocin Immunoreactivity in Goldfish Brains: Characterizing Primitive Circuits Associated with Social Regulation

“…All cell populations and terminal fields reported were observed in males and females in breeding and non-breeding conditions, although it is possible that quantification methods could have revealed sexual and/or seasonal differences in cell number such as those observed in medaka [Ohya and Hayashi, 2006]. However, Parhar et al [2001] reported no sexual dimorphisms in VT cell density in goldfish, and our behavioral data indicate that central VT and a VT antagonist similarly inhibit and stimulate social approach responses, respectively, in males and females [Thompson et al, 2008;unpubl. data].…”

“…Because approach/withdrawal processes underlie most social interactions in vertebrates, discovering the neural circuits associated with such influences could help elucidate a fundamental, potentially primitive mechanism through which this peptide controls social behavior. In fact, VT's ability to inhibit social approach in goldfish appears to depend upon a very primitive pathway in vertebrates: the preoptic projection to the hindbrain [Thompson et al, 2008]. The present study was conducted to further characterize hindbrain projection patterns associated with the regulation of social approach and to describe other pathways in the goldfish brain that might also participate in social regulation.…”

Dynamic neuromodulation of aggression by vasotocin: influence of social context and social phenotype in territorial songbirds

“…For instance, in several species of fish, subordinate/non-territorial male phenotypes exhibit significantly higher levels of VT mRNA or greater VT immunoreactivity relative to dominant/ territorial males (Grober et al 2002;Miranda et al 2003;Larson et al 2006;Lema 2006;Greenwood et al 2008). Parvocellular preoptic neurons also inhibit the social approach in fish via projections to the brainstem and a complex feedback loop through the periphery (Thompson et al 2008) and subordinate male mice exhibit significantly higher levels of VP-Fos colocalization in the PVN than do dominant males (J. M. Ho, G. E. Demas & J. L. Goodson, unpublished observation). The present results may therefore be informative for a wide range of taxa.…”