A method for calculating psychophysical performance limits based on stochastic neural responses is introduced and compared to previous analytical methods for evaluating auditory discrimination of tone frequency and level. The method uses signal detection theory and a computational model for a population of auditory nerve (AN) fiber responses. The use of computational models allows predictions to be made over a wider parameter range and with more complete descriptions of AN responses than in analytical models. Performance based on AN discharge times (all-information) is compared to performance based only on discharge counts (rate-place). After the method is verified over the range of parameters for which previous analytical models are applicable, the parameter space is then extended. For example, a computational model of AN activity that extends to high frequencies is used to explore the common belief that rate-place information is responsible for frequency encoding at high frequencies due to the rolloff in AN phase locking above 2 kHz. This rolloff is thought to eliminate temporal information at high frequencies. Contrary to this belief, results of this analysis show that rate-place predictions for frequency discrimination are inconsistent with human performance in the dependence on frequency for high frequencies and that there is significant temporal information in the AN up to at least 10 kHz. In fact, the all-information predictions match the functional dependence of human performance on frequency, although optimal performance is much better than human performance. The use of computational AN models in this study provides new constraints on hypotheses of neural encoding of frequency in the auditory system; however, the method is limited to simple tasks with deterministic stimuli. A companion article in this issue (“Evaluating Auditory Performance Limits: II”) describes an extension of this approach to more complex tasks that include random variation of one parameter, for example, random-level variation, which is often used in psychophysics to test neural encoding hypotheses.

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