Prolonged low-level noise-induced plasticity in the peripheral and central auditory system of rats

Abstract

Prolonged low-level noise exposure alters loudness perception in humans, presumably by decreasing the gain of the central auditory system. Here we test the central gain hypothesis by measuring the acute and chronic physiologic changes at the level of the cochlea and inferior colliculus (IC) after a 75 dB SPL, 10–20 kHz noise exposure for 5 weeks. The compound action potential (CAP) and summating potential (SP) were used to assess the functional status of the cochlea and 16 channel electrodes were used to measure the local field potentials (LFP) and multi-unit spike discharge rates (SDR) from the IC immediately after and one-week post-exposure. Measurements obtained immediately post-exposure demonstrated a significant reduction in supra-threshold CAP amplitudes. In contrast to the periphery, sound-evoked activity in the IC was enhanced in a frequency-dependent manner consistent with models of enhanced central gain. Surprisingly, one-week post-exposure supra-threshold responses from the cochlea had not only recovered, but were significantly larger than normal, and thresholds were significantly better than controls. Moreover, sound-evoked hyperactivity in the IC was sustained within the noise exposure frequency band but suppressed at higher frequencies. When response amplitudes representing the neural output of the cochlea and IC activity at one-week post exposure were compared with control animal responses, a central attenuation phenomenon becomes evident, which may play a key role in understanding why low-level noise can sometimes ameliorate tinnitus and hyperacusis percepts.

Auditory central gain compensates for changes in cochlear output after prolonged low-level noise exposure

“…Animals were exposed to a 10–20 kHz octave-band noise presented at a total integrated intensity level of 65 dB SPL. The noise was generated and presented in an identical manner to our previously published study [33]. Briefly, the noise was generated using a Tucker Davis Technology RP2 real-time processor, sent to a power amplifier, then routed to a loudspeaker suspended with wire mesh above the animals cage.…”

“…Details of our methods for acquiring and analyzing the CAP can be found in previous publications [33, 34]. Briefly, animals were placed in a customized head-holder, the right bulla was exposed and a small fistula was made to access the cochlear round window.…”

“…In contrast, reports using an exposure consisting of tone-pips (68–72 dB) to create an enriched acoustic environment depressed sound evoked responses in the auditory cortex without causing hearing loss [26]. Recently, we reported that a continuous low-level, octave band noise (10–20 kHz, 75 dB SPL), an intensity level similar to highway traffic, significantly reduced the amplitude of rat cochlear compound action potentials (CAPs), but elevated sound-evoked activity in the inferior colliculus (IC), indicating enhanced central gain [33]. Interestingly, at one-week post-exposure, CAP amplitudes were slightly enhanced, and sound-evoked IC responses partially recovered toward normal levels [33].…”

“…Recently, we reported that a continuous low-level, octave band noise (10–20 kHz, 75 dB SPL), an intensity level similar to highway traffic, significantly reduced the amplitude of rat cochlear compound action potentials (CAPs), but elevated sound-evoked activity in the inferior colliculus (IC), indicating enhanced central gain [33]. Interestingly, at one-week post-exposure, CAP amplitudes were slightly enhanced, and sound-evoked IC responses partially recovered toward normal levels [33]. These observations suggest that continuous exposure to low-level noise may provoke a sequence of cochlear mediated central gain changes in response to prolonged changes in acoustic experience.…”

Hidden cochlear impairments

“…Long-term exposure to the ambient noise is increasingly being recognized as a serious public health problem (Babisch et al., 2005; Babisch, 2008; Bodin et al., 2009; Bendokiene et al., 2011; van Kempen and Babisch, 2012). Our recent studies reveal that prolonged exposure to noise at ambient or environmental intensity levels (below 85 dB SPL) can significantly reduce peripheral auditory function (Chen et al., 2014, 2018; Sheppard et al., 2017). In the cochlear region above the noise band, long-term low-level noise exposure (18–24 kHz at 85 dB SPL for 6 weeks) selectively reduced the cochlear output (CAP) at the high stimulation levels but did not affect the CAP-threshold, possibly reflecting the loss of the synapses at high-threshold fibers.…”