Proceedings of the National Academy of Sciences | 2019
Corticobasal ganglia projecting neurons are required for juvenile vocal learning but not for adult vocal plasticity in songbirds
Abstract
Significance We addressed the question, “How do corticobasal ganglia projecting neurons contribute to vocal learning?” We performed specific ablation of the vocal cortical neurons projecting to the basal ganglia, HVC(X) neurons in a songbird, which generate temporally precise firing during singing. Specific ablation of HVC(X) neurons in juveniles caused deficits in learning the tutor song’s acoustics and less consistency of song sequence. In contrast, adult HVC(X) neuron ablation did not affect the degree of vocal fluctuations or cause alteration in song structure by auditory feedback inhibition. These results support the hypothesis that HVC(X) neurons are a neural substrate for transferring temporal signals, but not for regulating vocal fluctuations or conveying auditory feedback, to the basal ganglia for vocal learning and maintenance. Birdsong, like human speech, consists of a sequence of temporally precise movements acquired through vocal learning. The learning of such sequential vocalizations depends on the neural function of the motor cortex and basal ganglia. However, it is unknown how the connections between cortical and basal ganglia components contribute to vocal motor skill learning, as mammalian motor cortices serve multiple types of motor action and most experimentally tractable animals do not exhibit vocal learning. Here, we leveraged the zebra finch, a songbird, as an animal model to explore the function of the connectivity between cortex-like (HVC) and basal ganglia (area X), connected by HVC(X) projection neurons with temporally precise firing during singing. By specifically ablating HVC(X) neurons, juvenile zebra finches failed to copy tutored syllable acoustics and developed temporally unstable songs with less sequence consistency. In contrast, HVC(X)-ablated adults did not alter their learned song structure, but generated acoustic fluctuations and responded to auditory feedback disruption by the introduction of song deterioration, as did normal adults. These results indicate that the corticobasal ganglia input is important for learning the acoustic and temporal aspects of song structure, but not for generating vocal fluctuations that contribute to the maintenance of an already learned vocal pattern.