DESCRIPTION (provided by applicant): The central goal of the research proposed here is to understand how the vertebrate auditory system is able to recognize and interpret an enormous repertoire of species-typical vocal communication signa's. Sound communication is not unique to humans, but rather is a trait shared with many non-mammalian vertebrates. The focus here is on sound producing! vocalizing teleost fish that provide model systems to identify the basic principles of neural operation that have lead to the evolution of the complex auditory system of mammals, including humans. Vocalizing teleosts have a simple repertoire of species-typical signals central to their social and reproductive behavior. These signals can be easily reproduced and individuals produce stereotyped behavioral responses to playbacks of natural or computer-synthesized signals. Teleosts also have a central auditory system resembling that of terrestrial vertebrates including mammals. We propose that the plainfin midshipman fish (Porichthys notatus) has the vocal and acoustic behaviors, and underlying neural encoding mechanisms and circuitry, both necessary and sufficient to solve acoustic problems that challenge all vertebrates. Midshipman fish, in particular, produce advertisement and agonistic vocalizations with highly divergent physical attributes. Males acoustically court females using hums that are long duration (secs-l h) and exhibit an essentially flat envelope consisting of a low fundamental frequency (90-100 Hz) and several harmonics. In contrast, males also emit agonistic signal with envelope modulations, namely brief (50-200 ms) grunts at intervals of 2-3 Hz (grunts have FOs like hums). Envelope modulations are also introduced when the hums of two males overlap to produce an acoustic beat with a small difference frequency (0-8 Hz) determined by the difference in the two FOs. Behavioral studies show that individual midshipman distinguish hums from non-hums (beats and grunt-hke pulse trains) based on signal duration, silent gaps between signals and the degree of envelope modulation. Three specific aims will investigate how auditory mechanisms provide a neural basis for the behavioral categorization of hums from non-hums. Aim 1 uses physiological measures (spike rate and synchronization) and stimuli that mimic natural vocalizations to investigate brainstem encoding mechanisms for categorizing acoustic signals as either hums or non-hums. Aim 2 will couple these neurophysiological measures with extracellular and intracellular dye labeling to delineate the functional circuitry of the neurons identified in Aim 1. Aim 3 will investigate seasonal, reproductive state-dependent plasticity responsible for differential processing in the peripheral and central auditory systems.