Identification of a forebrain motor programming network for the learned song of zebra finches

Abstract

The stereotyped delivery of sequences of vocalizations by singing zebra finches is thought to be mediated by a “central motor program.” We hypothesized that electrically stimulating, and thus perturbing, the neural components of this motor program during singing should alter the subsequent singing pattern. In contrast, perturbing the activity of other neurons in the song motor pathway that do not participate directly in generating the song temporal pattern should not affect the singing pattern. We found that unilaterally stimulating the forebrain area RA of singing birds with chronically implanted electrodes distorted ongoing syllables without changing the order or timing of ensuing syllables. However, stimulating forebrain area HVc, which projects directly to RA, altered both ongoing syllables and the ensuing song pattern. These findings indicate that syllable sequencing during singing is organized in forebrain areas above RA (including HVc) and that the resulting pattern is imposed on lower structures of the motor pathway. Furthermore, the observation that unilateral forebrain perturbation was sufficient to alter the pattern of this bilaterally organized behavior suggests that (non-auditory) feedback pathways to the forebrain exist to coordinate the two hemispheres during singing. We suggest that the study of the motor control system for birdsong has provided the most direct evidence to date for localizing the programming of a skilled motor sequence to the telencephalon.