Seasonal plasticity of song behavior relies on motor and syntactic variability induced by a basal ganglia-forebrain circuit

The plasticity of nervous systems allows animals to quickly adapt to a changing environment. In particular, seasonal plasticity of brain structure and behavior is often critical to survival or mating in seasonal climates. Songbirds provide striking examples of seasonal changes in neural circuits and vocal behavior and have emerged as a leading model for adult brain plasticity. While seasonal plasticity and the well-characterized process of juvenile song learning may share common neural mechanisms, the extent of their similarity remains unclear. Especially, it is unknown whether the basal ganglia (BG)-forebrain loop which implements song learning in juveniles by driving vocal exploration participates in seasonal plasticity. To address this issue, we performed bilateral lesions of the output structure of the song-related BG-forebrain circuit (the magnocellular nucleus of the anterior nidopallium) in canaries during the breeding season, when song is most stereotyped, and just after resuming singing in early fall, when canaries sing their most variable songs and may produce new syllable types. Lesions drastically reduced song acoustic variability, increased song and phrase duration, and decreased syntax variability in early fall, reverting at least partially seasonal changes observed between the breeding season and early fall. On the contrary, lesions did not affect singing behavior during the breeding season. Our results therefore indicate that the BG-forebrain pathway introduces acoustic and syntactic variability in song when canaries resume singing in early fall. We propose that BG-forebrain circuits actively participate in seasonal plasticity by injecting variability in behavior during non-breeding season.

Significance statement: The study of seasonal plasticity in temperate songbirds has provided important insights into the mechanisms of structural and functional plasticity in the central nervous system. The precise function and mechanisms of seasonal song plasticity however remain poorly understood. We show here that a basal ganglia-forebrain circuit involved in the acquisition and maintenance of birdsong is actively inducing song variability outside the breeding season, when singing is most variable, while having little effect on the stereotyped singing during the breeding season. Our results suggest that seasonal plasticity reflects an active song-maintenance process akin to juvenile learning, and that basal ganglia-forebrain circuits can drive plasticity in a learned vocal behavior during the non-injury-induced degeneration and reconstruction of the neural circuit underlying its production.