Topographic organization of a forebrain pathway involved with vocal learning in zebra finches.

Abstract

A serial pathway from a thalamic nucleus (DLM; the medial portion of the dorsolateral nucleus of the anterior thalamus) to a cortical region (lMAN; the lateral magnocellular nucleus of the anterior neostriatum) to a motor-cortical region (RA; the robust nucleus of the archistriatum) is necessary for vocal production during song learning in juvenile zebra finches but not for the recitation of a song already learned by adults. To obtain new information about the possible function of the DLM-->lMAN-->RA pathway in vocal learning, we used anterograde and retrograde tract-tracing techniques (pressure injections of DiI and DiA) to map the pattern of axonal connections between these brain regions in adult male zebra finches. Results revealed two topographically organized pathways that traverse the songbird forebrain in parallel. An oval-shaped dorsal/lateral portion of DLM projects solely to the central core of lMAN (lMANcore), whereas a crescent-shaped region, including ventral and medial DLM, projects exclusively to a parvicellular shell that encircles lMANcore (lMANshell). In turn, lMANshell neurons project solely to an arc-shaped region of dorsal archistriatum just lateral to RA (Ad; archistriatum, pars dorsalis), whereas lMANcore neurons project exclusively to RA. We also identified crossed and reciprocal pathways between lMANcore/shell and the lateral portion of the ventral archistriatum, which may contribute to interhemispheric coordination of vocal behavior. A robust topographic organization was observed in the axonal projections from dorsal/lateral-DLM-->lMANcore-->RA and from ventral/medial-DLM-->lMANshell-->Ad, raising the question of what is being mapped within these two forebrain pathways. Because RA projection neurons are organized myotopically with respect to the major vocal (syringeal) muscles (D.S. Vicario, 1991, J. Comp. Neurol. 309:486-494), one possibility is that a mapping of vocal/expiratory musculature is preserved "upstream" within these pathways. Similarly, the presence of song-selective auditory neurons in DLM, lMAN, and RA (A.J. Doupe and M. Konishi, 1991, Soc. Neurosci. Abstr. 18:527) suggests that these pathways might subserve some form of auditory or auditory-motor mapping.