Early corticosterone increases vocal complexity in a wild parrot: An organizational role of the hypothalamic-pituitary-adrenal axis in vocal learning?

The neuroendocrinology of vocal learning is exceptionally well known in passerine songbirds. Despite huge life history, genetic and ecological variation across passerines, song learning tends to occur as a result of rises in gonadal and non-gonadal sex steroids that shape telencephalic vocal control circuits and song. Parrots are closely related but independently evolved different cerebral circuits for vocal repertoire acquisition in both sexes that serve a broader suite of social functions and do not appear to be shaped by early androgens or estrogens; instead, parrots begin a plastic phase in vocal development at an earlier life history stage that favors the growth, maturation, and survival functions of corticosteroids. As evidence, corticosterone (CORT) supplements given to wild green-rumped parrotlets (Forpus passerinus) during the first week of vocal babbling resulted in larger vocal repertoires in both sexes in the remaining days before fledging. Here, we replicate this experiment but began treatment 1 week before in development, analyzing both experiments in one model and a stronger test of the organizational effects of CORT on repertoire acquisition. Early CORT treatment resulted in significantly larger repertoires compared to late treatment. Both treatment groups showed weak negative effects on the early, reduplicated stage of babbling and strong, positive effects of CORT on the later, variegated stage. Results are consistent with more formative effects of corticosteroids at earlier developmental stages and a role of the hypothalamic-pituitary-adrenal axis (HPA) in vocal repertoire acquisition. Given the early emergence of speech in human ontogeny, parrots are a promising model for understanding the putative role of the HPA axis in the construction of neural circuits that support language acquisition. This work shows that week-long corticosterone supplements given to pre-endothermic nestling parrots resulted in larger vocal repertoires than controls more than a week after treatment ended, and larger repertoires than a previous study where CORT was administered a week later in development. Results strongly suggest early, organizational effects of corticosteroids on vocal production learning and a beneficial role of the Hypothalamic-Pituitary-Adrenal axis in the development of complex social communication. This represents adeparture from the songbird model and the experimental support for the putative endocrine pathway that supports language precursors in human infants.image