Hyperexcitability of inferior colliculus neurons caused by acute noise exposure

Niu, Yuguang; Kumaraguru, Anand; Wang, Rongguang; Sun, Wei

doi:10.1002/jnr.23152

Cited by 35 publications

(24 citation statements)

References 17 publications

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“…Neurophysiological studies in animals have shown increased neural activity in the central auditory system following acoustic trauma in various regions including the cochlear nucleus, inferior colliculus, and auditory cortex (e.g. Finlayson and Kaltenbach, 2009; Mulders and Robertson, 2009; Seki and Eggermont, 2003; Niu et al 2013). Recent studies in humans also point to an increase in the gain of central auditory neurons with auditory pathology.…”

Section: Discussionmentioning

confidence: 99%

Sensorineural hearing loss amplifies neural coding of envelope information in the central auditory system of chinchillas

Zhong¹,

Henry²,

Heinz³

2014

Hearing Research

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People with sensorineural hearing loss often have substantial difficulty understanding speech under challenging listening conditions. Behavioral studies suggest that reduced sensitivity to the temporal structure of sound may be responsible, but underlying neurophysiological pathologies are incompletely understood. Here, we investigate the effects of noise-induced hearing loss on coding of envelope (ENV) structure in the central auditory system of anesthetized chinchillas. ENV coding was evaluated noninvasively using auditory evoked potentials recorded from the scalp surface in response to sinusoidally amplitude modulated tones with carrier frequencies of 1, 2, 4, and 8 kHz and a modulation frequency of 140 Hz. Stimuli were presented in quiet and in three levels of white background noise. The latency of scalp-recorded ENV responses was consistent with generation in the auditory midbrain. Hearing loss amplified neural coding of ENV at carrier frequencies of 2 kHz and above. This result may reflect enhanced ENV coding from the periphery and/or an increase in the gain of central auditory neurons. In contrast to expectations, hearing loss was not associated with a stronger adverse effect of increasing masker intensity on ENV coding. The exaggerated neural representation of ENV information shown here at the level of the auditory midbrain helps to explain previous findings of enhanced sensitivity to amplitude modulation in people with hearing loss under some conditions. Furthermore, amplified ENV coding may potentially contribute to speech perception problems in people with cochlear hearing loss by acting as a distraction from more salient acoustic cues, particularly in fluctuating backgrounds.

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Section: Discussionmentioning

confidence: 99%

Sensorineural hearing loss amplifies neural coding of envelope information in the central auditory system of chinchillas

Zhong¹,

Henry²,

Heinz³

2014

Hearing Research

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“…Existing theories suggest a potential involvement of both peripheral and/or central mechanisms (Wrinch, 1909;Baguley and Andersson, 2007;Niu et al, 2013). The lack of an animal model of hyperacusis makes it difficult to prove the validity of any postulated mechanisms responsible for this condition.…”

Section: Mechanismsmentioning

confidence: 99%

Decreased sound tolerance

Jastreboff

Jastreboff²

2015

Handbook of Clinical Neurology

100

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“…Reduced excitability following noise exposure is also found in the auditory cortex (Insanally, Albanna, & Bao, ; Noreña, Tomita, & Eggermont, ), in the cochlear nucleus (Pilati et al., ), in the IC following juvenile overexposure (Bureš, Grécová, Popelář, & Syka, ), and in a previous study from our lab using the same noise exposure paradigm (Heeringa & van Dijk, ). However, enhanced excitability in the IC following acoustic trauma has also been reported (Niu et al., ; Salvi, Saunders, Gratton, Arehole, & Powers, ). This discrepancy can be explained by several factors, including the type of acoustic trauma (tonal vs. noise, unilateral vs. bilateral, temporary vs. permanent threshold shift), the species and the recovery time, and may need additional research to further elucidate.…”

Section: Discussionmentioning

confidence: 90%

“…This hypothesis considers that steeper RLFs result in greater variation of firing rates when the level of the acoustic stimulus varies, similar to amplitude fluctuations of the sound envelope, and as such increase the synchronization index. In the IC, steeper RLFs are evident immediately after acoustic trauma (Niu, Kumaraguru, Wang, & Sun, ). Furthermore, loss of inhibitory networks can result in steeper RLFs (Caspary, Schatteman, & Hughes, ; Kuenzel, Nerlich, Wagner, Rübsamen, & Milenkovic, ; Pollak & Park, ; Sivaramakrishnan et al., ) and thus can be involved in the observed increased response gains in low‐CF units following acoustic trauma.…”

Section: Discussionmentioning

confidence: 99%

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

Heeringa

Dijk

2018

Eur J of Neuroscience

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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.

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Hyperexcitability of inferior colliculus neurons caused by acute noise exposure

Cited by 35 publications

References 17 publications

Sensorineural hearing loss amplifies neural coding of envelope information in the central auditory system of chinchillas

Sensorineural hearing loss amplifies neural coding of envelope information in the central auditory system of chinchillas

Decreased sound tolerance

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

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