Behavioral and Molecular Characterization of the Early Phase in Vocal Learning in the Zebra Finch

Abstract

Similar to the development of speech in human infants, song learning in juvenile songbirds starts with memorization of adult vocalizations. Young birds develop their own song as a replica of a memorized adult song model through trial and error learning through abundant vocal practice. The internal model of this adult song, termed the ‘template’ is therefore central for guiding the process of vocal learning. However, even the most fundamental aspects of the template, such as when, where and how it is encoded in the brain, remain poorly understood. This dissertation attempts to define a paradigm where the onset of vocal learning and template formation can be time-locked to a small window of exposure to the tutor song. Using this paradigm, I further characterize the molecular changes accompanying the initial phase of vocal learning.

The work described here shows that, in the zebra finch, template encoding can be time locked to, on average, a two-hour period of juvenile life and based on just 75 seconds of cumulative tutor song exposure. Rapid changes in vocal output induced by this exposure can be used as markers for predicting the future success of song imitation. To investigate the brain regions involved in this initial phase of vocal learning, a new approach was developed to interrogate global patterns of activity induced gene expression. Statistical parametric mapping, a method used for analysis of functional activity, was adapted to analyze regional activation across 3D reconstructions of whole brain gene expression maps. Using this approach, regions engaged at different stages of vocal learning were identified. To track the molecular mechanisms underlying these activation patterns, changes in the transcriptome of specific brain nuclei were analyzed as the young males undergo rapid changes in the vocal output in response to training. Significant changes in gene expression patterns were detected with divergent gene expression patterns across individual brain regions.

The behavioral and molecular tools developed here present an important advance for understanding how the template is instantiated in the songbird brain.