The immediate effects of acoustic trauma on excitation and inhibition in the inferior colliculus: A Wiener-kernel analysis

Abstract

Noise-induced tinnitus and hyperacusis are thought to correspond to a disrupted balance between excitation and inhibition in the central auditory system. Excitation and inhibition are often studied using pure tones; however, these responses do not reveal inhibition within the excitatory pass band. Therefore, we used a Wiener-kernel analysis, complemented with singular value decomposition (SVD), to investigate the immediate effects of acoustic trauma on excitation and inhibition in the inferior colliculus (IC).Neural responses were recorded from the IC of three anesthetized albino guinea pigs before and immediately after a one-hour bilateral exposure to an 11-kHz tone of 124 dB SPL. Neural activity was recorded during the presentation of a 1-h continuous 70 dB SPL Gaussian-noise stimulus. Spike trains were subjected to Wiener-kernel analysis in which the second-order kernel was decomposed into excitatory and inhibitory components using SVD.Hearing thresholds between 3 and 22 kHz were elevated (13–47 dB) immediately after acoustic trauma. The presence and frequency tuning of excitation and inhibition in units with a low characteristic frequency (CF; < 3 kHz) was not affected, inhibition disappeared whereas excitation was not affected in mid-CF units (3 < CF < 11 kHz), and both excitation and inhibition disappeared in high-CF units (CF > 11 kHz). This specific differentiation could not be identified by tone-evoked receptive-field analysis, in which inhibitory responses disappeared in all units, along with excitatory responses in high-CF units.This study is the first to apply Wiener-kernel analysis, complemented with SVD, to study the effects of acoustic trauma on spike trains derived from the IC. With this analysis, a reduction of inhibition and preservation of good response thresholds was shown in mid-CF units immediately after acoustic trauma. These neurons may mediate noise-induced tinnitus and/or hyperacusis. Moreover, an immediate profound high-frequency hearing loss was reflected by reduced evoked firing rates and loss of both excitation and inhibition in high-CF units.