Nonlinear Spectrotemporal Sound Analysis by Neurons in the Auditory Midbrain

The auditory system of humans and animals must process information from sounds that dynamically vary along multiple stimulus dimensions, including time, frequency, and intensity. Therefore, to understand neuronal mechanisms underlying acoustic processing in the central auditory pathway, it is essential to characterize how spectral and temporal acoustic dimensions are jointly processed by the brain. We use acoustic signals with a structurally rich time-varying spectrum to study linear and nonlinear spectrotemporal interactions in the central nucleus of the inferior colliculus (ICC). Our stimuli, the dynamic moving ripple (DMR) and ripple noise (RN), allow us to systematically characterize response attributes with the spectrotemporal receptive field (STRF) methods to a rich and dynamic stimulus ensemble. Theoretically, we expect that STRFs derived with DMR and RN would be identical for a linear integrating neuron, and we find that ∼60% of ICC neurons meet this basic requirement. We find that the remaining neurons are distinctly nonlinear; these could either respond selectively to DMR or produce no STRFs despite selective activation to spectrotemporal acoustic attributes. Our findings delineate rules for spectrotemporal integration in the ICC that cannot be accounted for by conventional linear–energy integration models.