The Development of Connectivity and the Nature of Synaptic Transmission between Avian Song Control Nuclei

Song is a learned vocalization unique to passerine birds. Young songbirds hear and memorize their father's song and then, as they mature, match their own song to the memorized model using auditory feedback. Song is controlled by a specialized neural circuit in the songbird's brain. The primary song control circuit is involved in vocal motor control, and is essential to song production in the adult. An "accessory" portion of the circuit appears unnecessary for adult song production, but is required for normal song development. The discrete nature of the song circuit, plus the stereotyped nature of song development, promise that the acquisition and refinement of a learned behavior can be understood on a cellular level. The robust nucleus of the archistriatum (RA), located in the songbird's caudal forebrain, is part of the primary pathway, and projects to motoneurons innervating the vocal musculature. RA is innervated by nucleus HVc, another primary structure, and by nucleus MAN, part of the accessory pathway. This study examines the changes in connectivity and the nature of synaptic transmission between these nuclei during development. MAN terminals were present within RA fifteen days after hatching, although HVc axons did not enter the nucleus until ten days later. The physiology of MAN and HVc synapses within RA was examined in an in vitro brain slice preparation. Before day 25, stimulation of MAN, but not HVc, fibers evoked excitatory synaptic potentials from virtually all RA neurons. MAN EPSPs were glutamatergic and activated NMDA-receptors on RA neurons. In slices prepared from male birds 40 to 70 days old, stimulation of MAN and HVc fibers evoked synaptic responses from most RA neurons. The properties of MAN EPSPs resembled those observed before day 25. Unlike the MAN EPSPs, HVc EPSPs were largely mediated by non-NMDA glutamate receptors. Both EPSPs could be enhanced for long periods of time by certain patterns of electrical stimulation. Therefore, connections important to song development form before those essential to adult song production. These two pathways exhibit distinct pharmacological properties that may be related to their specific roles in song acquisition and production.