Nonlinear response properties in the inferior colliculus: Common sound-frequency dependence for linear and nonlinear responses

TL;DR

This study investigates the linear and nonlinear sound response properties of neurons in the cat inferior colliculus using reverse correlation with dynamic moving ripple stimuli, revealing nonlinearities are prevalent and frequency-dependent.

Contribution

It provides the first detailed characterization of nonlinear response properties in ICC neurons, showing they are common and primarily occur at preferred frequencies.

Findings

Over half of the neurons show significant nonlinear responses.

Nonlinearities are most prominent at the neurons' best frequency.

Nonlinear preferences can match or oppose linear response patterns.

Abstract

Neurons in the main center of convergence in the auditory midbrain, the central nucleus of the inferior colliculus (ICC) have been shown to display either linear significant receptive fields, or both, linear and nonlinear significant receptive fields. In this study, we used reverse correlation to probe linear and nonlinear response properties of single neurons in the cat ICC. The receptive fields display areas of stimulus parameters leading to enhanced or inhibited spiking activity, and thus allow investigating the interplay to process complex sounds. Spiking responses were obtained from neural recordings of anesthetized cats in response to dynamic moving ripple (DMR) stimuli. The DMR sound contains amplitude and frequency modulations and allows systematically mapping neural preferences. Correlations of the stimulus envelope that preferably excite neurons can be mapped with the spike-triggered covariance. The spike-triggered average and -covariance were computed for the envelope of the DMR, separately for each frequency carrier (spanning a range of 0-5.5 octaves). This enables studying processing of the sound envelope, and to investigate whether nonlinearities are more pronounced at the neurons' preferred frequencies rather than at other frequencies. We find that more than half of the neurons (n=120) display significant nonlinear response properties at least at one frequency carrier. Nonlinearities are dominant at the neuron's best frequency. The nonlinear preferences can have either the same or opposite temporal receptive field pattern (e.g. on-off) as the linear preferences. No relationship to other neural properties such as feature-selectivity, phase-locking, or the like has been found. Thus, these nonlinearities do not seem to be linked to a specific type of neuron but to be inherent to ICC neurons indicating a diverse range of filtering characteristics.