Millisecond-scale motor control precedes sensorimotor learning in Bengalese finches

A key goal of the nervous system in young animals is to learn motor skills. Songbirds learn to sing as juveniles, providing a unique opportunity to identify the neural correlates of skill acquisition. Prior studies have shown that spike rate variability decreases during song acquisition, suggesting a transition from rate-based neural control to the millisecond-precise motor codes known to underlie adult vocal performance. By quantifying how the ensemble of spike patterns fired by cortical neurons (the “neural vocabulary”) and the relationship between spike patterns and song acoustics (the “neural code”) change during song acquisition, we quantified how vocal control changes across learning in juvenile Bengalese finches. We found that despite the expected drop in rate variability (a learning-related change in spike vocabulary), the precision of the neural code in the youngest singers is the same as in adults, with 1–2 millisecond variations in spike timing transduced into quantifiably different behaviors. In contrast, fluctuations of firing rates on longer timescales fail to affect the motor output. The consistent presence of millisecond-scale motor coding during changing levels of spike rate and behavioral variability supports the view that variability early in learning stems from deliberate motor exploration rather than imprecise motor control.