Connections of a motor cortical region in zebra finches: relation to pathways for vocal learning.

The lateral magnocellular nucleus of the anterior neostriatum (lMAN) is necessary for both initial learning of vocal patterns in developing zebra finches, as well as for modification of adult song under some circumstances. Lateral MAN is composed of two subregions: a core of magnocellular neurons and a surrounding shell composed primarily of parvocellular neurons. Neurons in lMAN(core) project to a region of motor cortex known as robust nucleus of the archistriatum (RA), whereas neurons in lMAN(shell) project to a region adjacent to RA known as dorsal archistriatum (Ad). We studied the axonal connections of Ad in adult male zebra finches. In contrast to RA, Ad neurons make a large number of efferent projections, which do not include direct inputs to vocal or respiratory motor neurons. The major efferent projections of Ad are to: (1) the striatum of avian basal ganglia; (2) a dorsal thalamic zone (including the song-control nuclei dorsomedial nucleus of the posterior thalamus [DMP] and dorsolateral nucleus of the medial thalamus [DLM]); (3) restricted regions within the lateral hypothalamus (stratum cellulare externum [SCE]), which may also relay information to the same dorsal thalamic zone; (4) a nucleus in the caudal thalamus (medial spiriform nucleus [SpM]); (5) deep layers of the tectum, which project to the thalamic song-control nucleus Uva; (6) broad regions of pontine and midbrain reticular formation; and (7) areas within the ventral tegmental area and substantia nigra (ventral tegmental area [AVT], substantia nigra [SN]), which overlap with regions that project to Area X, a song-control nucleus of avian striatum. Inputs to Ad derive not only from lMAN(shell), but also from a large area of dorsolateral caudal neostriatum (dNCL), which also receives input from lMAN(shell). That is, lMAN(shell) neurons project directly to Ad, and also multisynaptically to Ad via dNCL. Double-labeling studies show that lMAN(shell) contains two different populations of projection neurons: one that projects to Ad and another to dNCL. These results are exciting for two main reasons. The first is that some of these projections represent potential closed-loop circuits that could relay information back to song-control nuclei of the telencephalon, possibly allowing diverse types of song-related information to be both integrated between loops and compared during the period of auditory-motor integration. Because both auditory experience with an adult (tutor) song pattern and auditory feedback are essential to vocal learning, closed-loop pathways could serve as comparator circuits in which efferent commands, auditory feedback, and the memory of the tutor song are compared in an iterative fashion to achieve a gradual refinement of vocal production until it matches the tutor song. In addition, these circuits seem to have a strong integrative and limbic flavor. That is, the axonal connections of Ad neurons clearly include regions that receive inputs not only from somatosensory, visual, and auditory areas of cortex, but also from limbic regions, suggesting that they may be involved in higher order sensory processing, arousal, and motivation.