Development of individual axon arbors in a thalamocortical circuit necessary for song learning in zebra finches

Abstract

Individual axon arbors within developing neural circuits are remodeled during restricted sensitive periods, leading to the emergence of precise patterns of connectivity and specialized adaptive behaviors. In male zebra finches, the circuit connecting the medial dorsolateral nucleus of the thalamus (DLM) and its cortical target, the lateral magnocellular nucleus of the anterior neostriatum (IMAN), is crucial for the acquisition of a normal vocal pattern during the sensitive period for song learning. The shell subregion of IMAN as well as the entire terminal field of DLM axons within IMAN undergo a striking increase in overall volume during early stages of vocal learning followed by an equally substantial decrease by adulthood, by which time birds have acquired stable song patterns. Because the total number of DLM neurons remains stable throughout this period, the dramatic changes within the overall DLM→IMAN circuit are presumably attributable to dynamic rearrangements at the level of individual DLM axon arbors over the course of vocal learning. To study such rearrangements directly, we reconstructed individual DLM axon arbors in three dimensions at different stages during vocal learning. Unlike axon arbors in other model systems, in which the number of branches increases during development, DLM arbors are unusual in that they have the greatest number of branches at the onset of vocal learning and undergo large-scale retraction during the sensitive period for song learning. Decreases in the degree of overlap between DLM arbors apparently contribute to the increased overall volume of the DLM→IMAN circuit during vocal learning. These developmental changes in DLM axon arbors occur at the height of the sensitive period for vocal learning, and hence may represent either a morphological correlate of song learning or a necessary prerequisite for acquisition of song.