Reafferent thalamo-"cortical" loops in the song system of oscine songbirds

Songbirds have a complex vocal repertoire, much of which is learned by imitation. The vocal motor system of songbirds includes a set of telencephalic pathways dedicated to the acquisition and production of learned song. The main vocal motor pathway goes from the high vocal center (HVC) to the robust nucleus of the archistriatum (RA), which in turn innervates mesencephalic and medullary nuclei involved in vocalization. We used neural tract tracers (biotinylated dextran amines, fluorescein‐ and rhodamine‐linked dextran amines, and Fluorogold) to show that RA of adult male canaries (Serinus canaria) and zebra finches (Taeniopygia guttata) sends an ipsilateral projection to the posterior portion of the dorsomedial thalamic nucleus (DMP). DMP projects to the medial portion of the magnocellular nucleus of the anterior neostriatum (mMAN), which is known to project to HVC, forming a feedback circuit. We also observed that the projection from DMP to mMAN is bilateral. Extracellular multi‐unit recordings from awake restrained subjects have demonstrated that mMAN has auditory responses that are selective for the bird's own song. These auditory responses are similar to responses recorded simultaneously in HVC, but with a longer latency, suggesting that mMAN receives auditory information from HVC through the circuit we have described. We also saw a weaker projection from RA to the medial part of the dorsolateral nucleus of the thalamus (DLM), which is known to project to the lateral portion of the magnocellular nucleus of the anterior neostriatum (lMAN). lMAN is known to project to RA, completing yet another feedback circuit; lMAN is also part of the anterior forebrain pathway, which plays an essential role in song learning. These thalamo‐telencephalic circuits are similar to thalamo‐cortical circuits found in mammalian motor systems, and we suggest that the signals carried by these loops may be important for song perception, song learning, song production, and/or the bilateral coordination of vocal motor commands. J. Comp. Neurol. 380:275–290, 1997. © 1997 Wiley‐Liss, Inc.