Auditory representation of the vocal repertoire in a songbird with multiple song types

Neural mechanisms for representing complex communication sounds must solve the problem of encoding multiple and potentially overlapping signals. Birdsong provides an excellent model for such processing, in that many songbird species produce multiple song types. Although auditory song representations in single song type species have been studied, how song is represented in the brains of species that sing multiple song types remains unknown. Here we examine song type representations in swamp sparrows (Melospiza georgiana), a multiple song type species, by making in vivo intracellular recordings from the telencephalic nucleus HVc, the major auditory-vocal interface in the songbird brain. These recordings show that single HVc relay neurons often generate action potentials to playback of only a single song type, even though synaptic inputs on these cells can be activated by playback of other song types in the bird's repertoire and songs of other birds. These subthreshold response patterns suggest that the song evoked action potential discharge of a single relay neuron is more selective than its presynaptic network. One component of this presynaptic network is likely to be in HVc, because multiple recordings from single birds show that different relay neurons can respond best to different song types, whereas single interneurons can generate action potentials to all song types in the bird's repertoire. These results show that single HVc neurons can generate song type-specific action potential responses, a feature that may facilitate the selective auditory encoding of multiple learned vocalizations in a single brain area.