Lesions Involving Medial Anterior Forebrain Pathway Circuitry Destabilize Phrase Timing in Adult Canary Song
Hulsey-Vincent, M. R.; Vengrovski, G. J.; Sova, E.; Gardner, T. J.
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Basal ganglia-thalamo-cortical circuits are essential for learning complex motor sequences, yet their roles in controlling flexible motor behavior remain poorly understood. The homologous songbird Anterior Forebrain Pathway (AFP) drives song motor learning and was previously thought not to play a role in song performance, as early lesion studies reported no detectable effect. This perspective is now debated, as newer results demonstrate effects in subsets of songbirds. Here, we revisit this question in adult canaries by performing bilateral excitotoxic lesions targeting the lateral and medial subdivisions of the AFP. To quantify behavioral changes across thousands of recorded canary songs, we developed a high-throughput annotation pipeline that extends a self-supervised vision transformer (TweetyBERT) with a supervised classification head, eliminating the memory bottleneck of UMAP-based clustering. This model enables phrase-level analysis across thousands of songs per bird. We find that lesions involving the medial AFP produce a stuttering-like behavior, defined here as a prolonged and variable syllable repetition before transition, resulting in a significant increase in the variability of phrase duration. This effect was strongest in birds with medial+lateral AFP involvement, and was not observed in birds with lateral-only AFP lesions. Phrase duration variability remained elevated across much of the post-lesion recording period and was accompanied by detectable changes in syllable acoustic structure. Our results implicate the medial AFP in the ongoing control of phrase duration in adult canary song, challenging the view that the AFP is dispensable once song is learned. These findings position the medial AFP as a tractable model for understanding how basal ganglia and cortical dynamics jointly maintain complex learned motor sequences.
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