Electrophysiological analysis of a songbird basal ganglia circuit essential for vocal plasticity

The discrete, interconnected nuclei of the songbird brain, collectively termed the song system, underlie the learning and production of song. Two main forebrain pathways have been identified that contribute to song production, learning, and adult plasticity. A posterior "motor pathway" including nucleus HVc (used as the proper name), the robust nucleus of the archistriatum (RA) and descending projections to the brainstem, is essential for song production. An "anterior forebrain pathway," arising from HVc, passing through area X of the lobus parolfactorius, the medial portion of the dorsolateral nucleus of the anterior thalamus and the lateral magnocellular nucleus of the anterior neostriatum, and finally terminating in RA, is essential for song learning and adult plasticity. The fact that the lobus parolfactorius is thought to form a part of the avian striatum implies several predictions for the connections of area X and for the properties of its neurons. Here, we review the existing anatomical and electrophysiological data bearing on the nature of area X as a striatal structure. In general, the data strongly favor the notion that area X is striatal. One set of observations, however, is at odds with that idea, and we provide and partially test the hypothesis that area X also contains a pallidal component. We discuss further tests of this idea and implications for thinking of the song system as a basal ganglia loop similar to that described in mammals.