Disconnection of a Basal Ganglia Circuit in Juvenile Songbirds Attenuates the Spectral Differentiation of Song Syllables

ABSTRACT: Similar to language acquisition by human infants, juvenile male zebra finches (Taeniopygia guttata) imitate an adult (tutor) song by transitioning from repetitive production of one or two undifferentiated protosyllables to the sequential production of a larger and spectrally heterogeneous set of syllables. The pri-mary motor region that controls learned song is driven by a confluence of input from two premotor pathways: a posterior pathway that encodes the adult song syllables and an anterior pathway that includes a basal ganglia (BG)-thalamo-cortical circuit. Similar to mammalian motor-learning systems, the songbird BG circuit is thought to be necessary for shaping juvenile vocal behav-iour (undifferentiated protosyllables) toward specific tar-gets (the tutor’s song syllables). Here, we tested the hypothesis that anterior pathway activity contributes to the process of protosyllable differentiation. Bilateral ablation of lateral magnocellular nucleus of the anterior nidopallium (LMAN) was used to disconnect BG cir-cuitry at ages before protosyllable production and differ-entiation. Comparison to surgical controls revealed that protosyllables fail to differentiate in birds that received juvenile LMAN ablation—the adult songs of birds with>80 % bilateral LMAN ablation consisted of only one or two syllables produced with the repetitive form and spec-tral structure that characterizes undifferentiated proto-syllables in normal juveniles. Our findings support a role for BG circuitry in shaping juvenile vocal behaviour toward the acoustic structure of the tutor song and sug-gest that posterior pathway function remains in an imma-ture “default ” state when developmental interaction with the anterior pathway is reduced or eliminated. VC 201