Intrinsic and Extrinsic Contributions to Auditory Selectivity in a Song Nucleus Critical for Vocal Plasticity

Abstract

The development, maintenance, and perception of learned vocalizations in songbirds are likely to require auditory neurons that respond selectively to song. Neurons with song-selective responses have been described in several brain nuclei critical to singing, but the mechanisms by which such response properties arise, are modified, and propagate are poorly understood. The lateral magnocellular nucleus of the anterior neostriatum (LMAN) is the output of an anterior forebrain pathway (AFP) essential for learning and maintenance of song, processes dependent on auditory feedback. Although neurons throughout this pathway respond selectively to auditory presentation of the bird's own song, LMAN is the last stage at which responses to this auditory information could be transformed before being transmitted to vocal motor areas, where such responses may influence vocal production. Indeed, previous extracellular studies have indicated that LMAN's auditory selectivity is greater than that at earlier stages of the AFP. To determine whether LMAN local circuitry transforms or simply relays song-related auditory information to vocal control neurons, it is essential to distinguish local from extrinsic contributions to LMAN's auditory selectivity. In vivo intracellular recordings from LMAN projection neurons, coupled with local circuit inactivation, reveal that much of LMAN's song selectivity is supplied by its extrinsic inputs, but selective blockade of GABA receptors indicates that local inhibition is required for the expression of song selectivity. Therefore, LMAN neurons receive highly song-selective information, but LMAN's local circuitry can mask these selective inputs, providing a mechanism for context-dependent auditory feedback.