Neural coding of the sound envelope is changed in the inferior colliculus immediately following acoustic trauma

• Published in: The European journal of neuroscience Vol. 49; no. 10; pp. 1220 - 1232
• Main Authors: Heeringa, Amarins N., van Dijk, Pim
• Format: Journal Article
• Language: English
• Published: France Wiley Subscription Services, Inc 01.05.2019
• Subjects: Acoustic Stimulation; Acoustics; amplitude modulation; Animals; Auditory Perception - physiology; Auditory system; Evoked Potentials, Auditory, Brain Stem; guinea pig; Guinea Pigs; Hearing loss; Hearing Loss, Noise-Induced - physiopathology; Hearing protection; Inferior Colliculi - physiology; Inferior colliculus; Information processing; Male; Neural coding; Neurons - physiology; Noise; noise‐induced hearing loss; rate coding; Signal Processing, Computer-Assisted; Speech; temporal coding; Temporal variations; Trauma; guinea pig; amplitude modulation; noise-induced hearing loss; temporal coding; rate coding
• ISSN: 0953-816X; 1460-9568; 1460-9568
• DOI: 10.1111/ejn.14299

Sensorineural hearing loss is often accompanied by difficulties with understanding speech in fluctuating backgrounds, suggesting that neural coding of complex sound features, such as the sound envelope, is impaired. Here, we studied how temporal and rate coding of the envelope is affected in the inferior colliculus immediately after acoustic trauma. Neural activity in response to amplitude‐modulated noise was recorded from the inferior colliculus of the guinea pig, before and immediately after a 1‐hr 11‐kHz acoustic trauma. Units with a characteristic frequency (CF) below the trauma frequency (<11 kHz) showed increased response gains, a measure for temporal coding of the sound envelope, especially at low modulation frequencies (≤128 Hz). Units with a CF > 11 kHz, which had large acoustic trauma‐induced threshold shifts, had decreased response gains to amplitude‐modulated noise. Shapes of temporal modulation transfer functions shifted toward a higher proportion of low‐pass shapes in low‐CF units, and to less band‐pass shapes in high‐CF units. Furthermore, driven firing rates decreased, especially at high modulation frequencies for high‐CF units. The observed changes occurred immediately following trauma and were thus a result of the immediate trauma‐induced damage to the auditory system. If also present in human subjects, reduced response gains in high‐frequency units could disrupt coding of consonants and consequently impair speech understanding in noisy environments. Moreover, the enhanced temporal coding by low‐CF units of the low modulation frequencies could overly amplify responses to low‐frequency noise, further deteriorating listening in noise. We quantified the effects of acute acoustic trauma on encoding of amplitude modulations in the guinea pig inferior colliculus. Recording sites tuned below the exposure frequency showed enhanced temporal coding of amplitude modulations, whereas higher frequency sites showed diminished temporal coding. Temporal modulation transfer functions became more low‐pass shaped following acoustic trauma.