Development of Topography within Song Control Circuitry of Zebra Finches during the Sensitive Period for Song Learning

Abstract

Refinement of topographic maps during sensitive periods of development is a characteristic feature of diverse sensory and motor circuits in the nervous system. Within the neural system that controls vocal learning and behavior in zebra finches, axonal connections of the cortical nucleus lMAN demonstrate striking functional and morphological changes during vocal development in juvenile males. These circuits are uniquely important for song production during the sensitive period for vocal learning, and the overall size of these brain regions and their patterns of axonal connectivity undergo dramatic growth and regression during this time. Axonal connections to and from lMAN are topographically organized in adult males that have already learned song. We wondered whether the large-scale changes seen in lMAN circuitry during the time that vocal behavior is being learned and refined could be accompanied by the emergence of topographic mapping. However, results presented herein demonstrate that most of these song-control circuits show the same broad patterns of axonal connectivity between subregions of individual nuclei at the onset of song learning as seen in adult birds. Thus, coarse topographic organization is not dependent on the types of experience that are crucial for vocal learning. Furthermore, this maintenance of topographic organization throughout the period of song learning is clearly not achieved by maintenance of static axonal arbors. In fact, because the volumes of song-control nuclei are growing (or regressing), topography must be maintained by active remodeling of axonal arbors to adapt to the changes in overall size of postsynaptic targets. A salient exception to this pattern of conserved topography is the projection from lMAN to the motor cortical region RA: this pathway is diffusely organized at the onset of song learning but undergoes substantial refinement during early stages of song learning, suggesting that remodeling of axonal connections within this projection during the period of vocal learning may signify the production of increasingly refined vocal utterances.