Functional connectivity of the anterior forebrain pathway in the song system

The avian song system is the neural substrate underlying song learning and production. The anterior forebrain pathway (AFP) in the song system is regarded as a learning pathway, since lesions of this pathway in juveniles result in abnormal song development but lesions in adults do not disrupt songs. It consists of a loop serially connecting area X in the basal ganglia, the medial portion of the dorsolateral nucleus of the anterior thalamus (DLM) and the lateral portion of the magnocellular nucleus in the pallial area (lMAN). We want to test whether the AFP has neural mechanisms similar to those of the mammalian basal ganglia-thalamocortical pathway. Specifically, we want to examine in male zebra finches (1) whether the entire AFP is organized topographically and forms parallel, closed microscopic loops, (2) whether the area X → DLM projection is GABAergic, and (3) whether the DLM neurons have intrinsic properties similar to those of the mammalian thalamocortical neurons. By making small tracer injections into area X or lMAN, we found that the area X → DLM projection was topographic and confirmed the topography for other projections within the AFP. Quantification of the spatial mapping of all projections as well as dual-tram injections into corresponding areas in lMAN and area X strongly suggest that the AFP contains many closed, parallel loops. By combining immunostaining for glutamic acid decarboxylase with tract tracing or ibotenic acid lesion, we found that DLM receives a strong and the only GABAergic input from area X. In brain slices, we recorded juvenile or adult DLM neurons with whole-cell recording techniques. Stimulating afferent axons evoked strong monosynaptic; IPSPs that were completely blocked by the GABAA receptor blocker bicuculline methiodide. Most DLM neurons had intrinsic properties almost identical to those of mammalian thalamocortical neurons and these properties were largely maintained during the sensorimotor learning phase and in the adulthood. In summary, our studies show that the AFP is organized highly similarly to the mammalian basal ganglia-thalamocortical pathway at both macroscopic and cellular levels, suggesting that the AFP functions in song learning similarly to the mammalian basal ganglia pathway in sensorimotor learning