Functional identification of specialized basal ganglia circuits that regulate vocal motor sequences

Production of learned vocalizations requires precise selection and accurate sequencing of appropriate vocal-motor actions. The basal ganglia are essential for the selection and sequencing of motor actions, but the cellular specializations and circuit mechanisms governing accurate sequencing of vocalizations are unknown. Here, we use single-nucleus RNA sequencing and genetic manipulations to map basal ganglia cell types and circuits involved in the production of songbird vocal sequences. We identify cell-type specializations in direct-like and indirect-like basal ganglia pathways, including evolutionary expansion of striatal and arkypallidal cell-types that could facilitate vocal sequencing. Surprisingly, we find that FoxP2, a gene important for vocal development, can potently and reversibly control accurate sequencing of adult birdsong, and that phasic dopamine selectively regulates repetition of syllables independent of its role in reinforcement-based learning of how they are sung. These findings identify key evolutionary specializations and circuits essential for selection and sequencing of vocal-motor actions necessary for vocal communication.