The power of spoken language in communication is one of the defining adaptations of the human species, and it depends on the rapid production and perception of speech signals. Songbirds are the most easily studied of the few animal taxa that learn to produce vocal signals for social communication as humans do. Among songbirds, our knowledge of the zebra finch is most advanced. This application proposes to use the properties of auditory neurons in the songbird forebrain to investigate basic neural processes that serve discrimination and memory for auditory communication signals. Young male zebra finches learn their vocalizations from adult tutors through a process of imitation that resembles human speech acquisition. These vocalizations become stereotyped in adulthood and are unique to each individual, providing rich material for quantitative study of the brain processes that serve this natural communication system. Using neurophysiological recording in a forebrain auditory area, the caudo-medial nidopallium (NCM), the P.I. has demonstrated a neuronal form of recognition memory that lasts longer for conspecific than for heterospecific vocal sounds. These long-lasting memories discriminate the unique vocalizations of individual conspecifics, suggesting that NCM plays a special role in processing vocal signals. The significant acoustic and temporal features that distinguish sounds for NCM neurons can be assessed because, in this preparation, repeated presentation of a novel sound results in rapid, quantifiable decreases of the sensory response. When a different sound is presented, the response returns to its initial high level. This is a form of stimulus specific adaptation, reminiscent of similar processes described for the mammalian auditory cortex. The P.I. now proposes to record from NCM in awake zebra finches with advanced physiological methods, including acute and chronic multi-electrode recording, to determine 1) the detailed changes in neural response pattern that accompany memorization of a specific sound signal;2) the temporal rules that govern the neural processing of more complex sounds composed of syllable sequences, as occurs in song;and 3) the way in which this auditory recognition and memory system is engaged during real-time interaction with conspecifics. The results will not only provide a quantitative description of auditory processing for behaviorally relevant signals in songbirds, but will also shed light on neural processes that link rapid sound sequences into recognizable auditory objects. This is a basic step in decoding speech, as well as song, so these studies may provide useful models for normal and pathological speech processing in humans.
