The central goal of the research proposed here is to understand how the vertebrate auditory system recognizes and interprets an enormous repertoire of species-typical vocal communication signals. The establishment of non-mammalian models of acoustic communication provide a unique and practical opportunity to identify the basic principles of neural operation that have led to the evolution of the complex auditory system of mammals including humans. Teleost fishes are the largest group of extant vertebrates and include vocalizing species with a simple vocal repertoire and a central auditory system resembling that of mammals. We propose that the plainfin midshipman fish (Porichthys notatus) has the vocal and acoustic behaviors, and underlying neural mechanisms and circuitry, both necessary and sufficient to solve acoustic problems that challenge all vertebrates including the separation of simultaneous (concurrent) vocalizations. Male midshipman fish vocalize simultaneously while they court females using multi-harmonic advertisement calls. Three questions will address mechanisms for the encoding and decoding of individual and concurrent vocal signals: (1) How and where are concurrent vocal signals segregated and encoded by the nervous system? Single unit recordings in the eighth nerve and auditory midbrain will characterize responses to both simple signals such as two tone beats and single multi-harmonic signals, and more complex stimuli such as two or more concurrent multi-harmonic signals. Central recordings together with neuroanatomical (biocytin) tract-tracing will map the circuitry that subserves the auditory coding mechanisms identified. (2) How and where do auditory and vocal pathways interact before, during and after self-vocalization? Central vocal-acoustic pathways recently delineated in midshipman will now guide single unit studies that test hypotheses of the proposed role of vocal-acoustic circuitry in auditory coding mechanisms. (3) How does the temporal structure of a vocal signal influence information transmission by auditory nerve fibers? Information transmission measures the amount of information present in an afferent spike train (information rate) and the quality of the stimulus representation by a spike train (coding efficiency). The simplicity (2-3 harmonics) and long duration (up to 115 minutes) of the midshipman s advertisement call presents a unique opportunity to test the hypothesis that a vocal signal s temporal structure is exploited for optimizing information transmission and hence the recognition of individual concurrent vocal signals.
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