An avian basal ganglia pathway essential for vocal learning forms a closed topographic loop

Abstract

The mammalian basal ganglia-thalamocortical pathway is important for motor control, motor learning, and cognitive functions. It contains parallel, closed loops, at least some of which are organized topographically and in a modular manner. Songbirds have a circuit specialized for vocal learning, the anterior forebrain pathway (AFP), forming a basal ganglia loop with only three stations: the pallial ("cortex-like") lateral magnocellular nucleus of the anterior neostriatum (IMAN), the basal ganglia structure area X, and the medial portion of the dorsolateral thalamic nucleus (DLM). Several properties of this pathway resemble those of its mammalian counterpart, but it is unknown whether all projections in the loop are topographically organized, and if so, whether topography is maintained through the entire loop. After small single- or dual-tracer injections into area X and/or the IMAN of adult zebra finches, we found that the area X to DLM projection is topographically organized, and we confirmed the topography for all other AFP projections. Quantitative analysis suggests maintained topography throughout the loop. To test this directly, we injected different tracers into corresponding areas in IMAN and area X. We found somata retrogradely labeled from IMAN and terminals anterogradely labeled from area X occupying the same region of DLM. Many labeled somata were tightly surrounded by tracer-labeled terminals, indicating the microscopically closed nature of the AFP loop. Thus, like mammals, birds have at least one closed, topographic loop traversing the basal ganglia, thalamus, and pallium. Each such loop could serve as a computational unit for motor or cognitive functions.