This paper reviews the organizational principles and implications that have emerged from the analysis of HVc, a forebrain nucleus that is a major site of sensory, motor, and sensorimotor integration in the song control system of oscine passerine birds (songbirds). Anatomical, physiological, and behavioral data support the conclusion that HVc exists within a hierarchically organized system with parallel pathways that converge onto HVc. The organization of HVc is distributed and redundant, and its outputs exhibit broad divergence. A similar pattern of connectivity exists for neostriatum adjacent to HVc. This and other data support the hypothesis that the song system arose from an elaboration or duplication of pathways generally present in all birds. Spontaneous and auditory response activity is strongly correlated throughout HVc, with auditory responses exhibiting strong temporal modulation in a synchronized fashion throughout the nucleus. This suggests that the auditory representation of song is encoded in the synchronized temporal patterns of activation, and that the predominant selectivity for the individual's own song that is observed for HVc neurons results from interactions of auditory input with central pattern generators for song. Most, or all HVc neurons are recruited during singing. The auditory response and motor recruitment properties of individual HVc neurons have no simple relationship, and the spontaneous activity in HVc may build up in the seconds preceding a song. To the extent HVc participates in perceptual phenomena associated with song, production and perception are not tightly linked in adults but may be linked by shared developmental processes during periods of sensorimotor learning.