Teoh, H. K. | bioRxiv Science

bioRxiv2023

The songbird lateral habenula projects to dopaminergic midbrain and is important for normal vocal development

Mistakes in performance feel disappointing, suggesting that brain pathways for aversive feedback may play a role in motor learning. Here we tested if the lateral habenula (LHb), an evolutionarily conserved part of the limbic system known in mammals to relay aversive feedback from ventral pallidum (VP) to ventral tegmental area (VTA) dopamine neurons, is involved in birdsong learning and production. By combining viral tract tracing and functional circuit mapping, we discovered that songbird LHb links VP and an auditory cortical area to singing-related DA neurons that signal song errors. As in mammals, VP stimulation activated LHb activity and LHb stimulation suppressed DA firing. To test this pathways role in learning we lesioned the LHb in juvenile zebra finches and recorded their songs in adulthood. Birds with the LHb lesioned as juveniles produced highly unusual vocalizations as adults, including prolonged high-pitch notes and species-atypical trills. These findings identify a songbird VP-LHb-VTA pathway with similar functional connectivity as mammals, expand the known territories of vocal learning circuits, and demonstrate that limbic circuits associated with disappointing outcomes are important for motor performance learning.

neuroscience↗

bioRxiv2023

An anterior forebrain pathway in parrots is necessary for individual signatures of learned vocalizations

Parrots have enormous vocal imitation capacities and produce individually unique vocal signatures. Like songbirds, parrots have a nucleated neural song system with distinct anterior (AFP) and posterior forebrain pathways (PFP). To test if song systems of parrots and songbirds, which diverged over 50 million years ago, have a similar functional organization, we first established a neuroscience-compatible call-and-response behavioral paradigm to elicit learned contact calls in budgerigars (Melopsittacus undulatus). Using variational autoencoder-based machine learning methods, we show that contact calls within affiliated groups converge but that individuals maintain unique acoustic features, or vocal signatures, even after call convergence. Next, we transiently inactivated the outputs of AFP to test if learned vocalizations can be produced by the PFP alone. As in songbirds, AFP inactivation had an immediate effect on vocalizations, consistent with a premotor role. But in contrast to songbirds, where the isolated PFP is sufficient to produce stereotyped and acoustically normal vocalizations, isolation of the budgerigar PFP caused a degradation of call acoustic structure, stereotypy, and individual uniqueness. Thus the contribution of AFP and the capacity of isolated PFP to produce learned vocalizations have diverged substantially between songbirds and parrots, likely driven by their distinct behavioral ecology and neural connectivity.

neuroscience↗