The role of auditory experience in the formation of neural circuits underlying vocal learning in zebra finches

The initial establishment of topographic mapping within developing neural circuits is thought to be shaped by innate mechanisms and is primarily independent of experience. Additional refinement within topographic maps leads to precise matching between presynaptic and postsynaptic neurons and is thought to depend on experiential factors during specific sensitive periods in the animal's development. In male zebra finches, axonal projections of the cortical lateral magnocellular nucleus of the anterior neostriatum (lMAN) are critically important for vocal learning. Overall patterns of topographic organization in the majority of these circuits are adult-like throughout the sensitive period for vocal learning and remain stable despite large-scale functional and morphological changes. However, topographic organization within the projection from the core subregion of lMAN (lMAN(core)) to the motor cortical robust nucleus of the archistriatum (RA) is lacking at the onset of song development and emerges during the early stages of vocal learning. To study the effects of song-related experience on patterns of axonal connectivity within different song-control circuits, we disrupted song learning by deafening juvenile zebra finches or exposing them to loud white noise throughout the sensitive period for song learning. Depriving juvenile birds of normal auditory experience delayed the emergence of topographic specificity within the lMAN(core)-->RA circuit relative to age-matched controls, whereas topographic organization within all other projections to and from lMAN was not affected. The projection from lMANcore to RA therefore provides an unusual example of experience-dependent modification of large-scale patterns of brain circuitry, in the sense that auditory deprivation influences the development of overall topographic organization in this pathway.