Corticobasal ganglia projecting neurons are required for juvenile vocal learning but not for adult vocal plasticity in songbirds

Abstract

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.

Autism-linked gene FoxP1 selectively regulates the cultural transmission of learned vocalizations

“…The widespread expression of FoxP1 in striatal-projecting HVC X neurons is of interest because HVC X neurons are thought to provide timing cues to basal ganglia circuits involved in reinforcement-based motor imitation of song elements ( 28 , 38 , 43 – 46 ). In support of this view, lesions of HVC X neurons have recently been shown to significantly disrupt behavioral imitation of song in juvenile zebra finches ( 35 ); however, it is not known whether these learning deficits arise from problems in acquiring a memory during interactions with a song tutor or from problems in modifying song as juveniles practice singing.…”

“…3E : tutor exposure after FP1-KD, referred to as “social experience” group, FP1-KD SE) ( 19 ). Given the widespread expression of FoxP1 in striatal-projecting HVC X neurons, we hypothesized that FP1-KD might disrupt motor aspects of behavioral imitation of the tutors’ song ( 35 ). For example, it could impair a young bird’s ability to precisely modify song syllables to produce a good imitation of their tutor’s song.…”

Autism-linked gene FoxP1 selectively regulates the cultural transmission of learned vocalizations

“…HVC X neurons are thought to carry timing information about song to the basal ganglia, which facilitate accurate reinforcement-based imitation of syllables and sub-syllable elements 23-26 . In support of this view, genetic lesions of HVC X neurons have recently been shown to significantly disrupt behavioral imitation of song in juvenile male zebra finches 21 .…”

“…HVC X and HVC Av neurons transmit vocal motor-related signals to the striatum or auditory system, respectively. These two pathways are important for behavioral imitation of tutor-song in juvenile birds, but are not essential for song production in adult birds 19-21 . HVC RA neurons provide descending motor commands to the pallial nucleus RA, a connection which is necessary for the production of learned song at all stages of life 17,20,22 .…”

“…2a: tutoring pre-FP1-KD, referred to as ‘behavioral imitation’ group ( FP1-KD BI ), Fig.2e: tutoring post-FP1-KD, referred to as ‘social experience’ group ( FP1-KD SE )). Given the widespread expression of FoxP1 in striatal projecting HVC X neurons, we hypothesized that FP1-KD might disrupt behavioral imitation of the tutors’ song 21 . However, we found that FP1-KD after birds had an opportunity to form a memory of the tutor-song (FP1-KD BI birds) did not impact their ability to then copy that song during development (Fig.…”