Developmental effects of oxytocin neurons on social affiliation and processing of social information

Hormones regulate behavior either through activational effects that facilitate the acute expression of specific behaviors or through organizational effects that shape the development of the nervous system thereby altering adult behavior. The neurohormone oxytocin (OXT) has an activational role in several aspects of social behavior, including social processing, attention and reward, in rodents and humans. Previously, we showed that this activational role of OXT is evolutionarily conserved in deep time, since OXT also modulates perception of visual social cues and social recognition in zebrafish. In contrast, the organizational action of OXT neurons in maturation of distinct neural systems necessary for social behavior remains less explored. Here, we show that in zebrafish, OXT is required during early life for the display of social affiliation in adulthood. Perturbation of OXT neurons during early development led to a loss of dopaminergic neurons, associated with visual processing and reward, and altered the neuronal response to social stimuli in the preoptic area and the ventral telencephalon of the adult brain. Ultimately, adult fish which were ablated in early life, displayed altered functional connectivity within social decision-making brain nuclei both in naive state and in response to social stimulus and became less social. We propose that OXT neurons have an organizational role, namely to shape forebrain neuroarchitecture during development and to acquire an affiliative response towards conspecifics.