Vocal exploration is locally regulated during song learning.

Exploratory variability is essential for sensorimotor learning, but it is not known how and at what timescales it is regulated. We manipulated song learning in zebra finches to experimentally control the requirements for vocal exploration in different parts of their song. We first trained birds to perform a one-syllable song, and once they mastered it, we added a new syllable to the song model. Remarkably, when practicing the modified song, birds rapidly alternated between high and low acoustic variability to confine vocal exploration to the newly added syllable. Furthermore, even within syllables, acoustic variability changed independently across song elements that were only milliseconds apart. Analysis of the entire vocal output during learning revealed that the variability of each song element decreased as it approached the target, correlating with momentary local distance from the target and less so with the overall distance within a syllable. We conclude that vocal error is computed locally in subsyllabic timescales and that song elements can be learned and crystallized independently. Songbirds have dedicated brain circuitry for vocal babbling in the anterior forebrain pathway (AFP), which generates exploratory song patterns that drive premotor neurons at the song nucleus RA. We hypothesize that either AFP adjusts the gain of vocal exploration in fine timescales or that the sensitivity of RA premotor neurons to AFP/HVC inputs varies across song elements.