Magnified Neural Envelope Coding Predicts Deficits in Speech Perception in Noise

Abstract

Verbal communication in noisy backgrounds is challenging. Understanding speech in background noise that fluctuates in intensity over time is particularly difficult for hearing-impaired listeners with a sensorineural hearing loss (SNHL). The reduction in fast-acting cochlear compression associated with SNHL exaggerates the perceived fluctuations in intensity in amplitude-modulated sounds. SNHL-induced changes in the coding of amplitude-modulated sounds may have a detrimental effect on the ability of SNHL listeners to understand speech in the presence of modulated background noise. To date, direct evidence for a link between magnified envelope coding and deficits in speech identification in modulated noise has been absent. Here, magnetoencephalography was used to quantify the effects of SNHL on phase locking to the temporal envelope of modulated noise (envelope coding) in human auditory cortex. Our results show that SNHL enhances the amplitude of envelope coding in posteromedial auditory cortex, whereas it enhances the fidelity of envelope coding in posteromedial and posterolateral auditory cortex. This dissociation was more evident in the right hemisphere, demonstrating functional lateralization in enhanced envelope coding in SNHL listeners. However, enhanced envelope coding was not perceptually beneficial. Our results also show that both hearing thresholds and, to a lesser extent, magnified cortical envelope coding in left posteromedial auditory cortex predict speech identification in modulated background noise. We propose a framework in which magnified envelope coding in posteromedial auditory cortex disrupts the segregation of speech from background noise, leading to deficits in speech perception in modulated background noise.SIGNIFICANCE STATEMENT People with hearing loss struggle to follow conversations in noisy environments. Background noise that fluctuates in intensity over time poses a particular challenge. Using magnetoencephalography, we demonstrate anatomically distinct cortical representations of modulated noise in normal-hearing and hearing-impaired listeners. This work provides the first link among hearing thresholds, the amplitude of cortical representations of modulated sounds, and the ability to understand speech in modulated background noise. In light of previous work, we propose that magnified cortical representations of modulated sounds disrupt the separation of speech from modulated background noise in auditory cortex.

The effects of aging on neural signatures of temporal regularity processing in sounds

“…Although an increase in neural gain -which is thought to compensate for degraded inputs from the auditory periphery -may support the detection of weak signals (Gerken, 1979;Ernst and Moore, 2012;Chambers et al, 2016;Schlittenlacher and Moore, 2016), it may affect how a sound's regularity is represented in cortical structures, in an unhelpful way. This is in line with previous work demonstrating a correlation -with age partialed out -between neural gain enhancements and decreased speech perception performance in the presence of modulated background sound (Millman et al, 2017;Goossens et al, 2018), and with the observation that hearing loss increases the perceived magnitude of low-frequency amplitude modulation in sounds (Moore et al, 1996). This previous work together with the current findings indicate that neural function in central auditory brain structures of older people appears fundamentally altered, including, among others, a change in sensitivity to a sound's temporal regularity in auditory cortex and possibly in higher-level brain regions.…”

“…Previous source localizations suggest that synchronization of neural activity with low-frequency temporal regularities in sounds is strongest in auditory cortex (Herrmann et al, 2013a;Keitel et al, 2017;Millman et al, 2017). The finding of enhanced synchronization in auditory cortex for older people is consistent with the age-related gain enhancement that we observed using the adaptation paradigm.…”

“…Furthermore, an increase in neural gain appears to manifest as altered neural adaptation to sounds (Herrmann et al, 2016) and sound statistics (Herrmann et al, 2018), which may impair the flexible adjustment of perceptual systems to different acoustic environments, and may underlie the challenges older people experience with filtering out irrelevant information. Finally, an increase in neural gain in auditory cortex has been related to impaired speech perception (Millman et al, 2017;Goossens et al, 2018). Hence, despite older people showing enhanced responsivity to sound in auditory cortex, acoustic environments may not be represented accurately in the brain.…”

“…Sensitivity to temporal regularity in sounds can be assessed by the strength of neural synchronization (Purcell et al, 2004;Herrmann et al, 2013a;Goossens et al, 2016;Henry et al, 2017). Neural synchronization reflects the alignment of neural activity with periodicity in sound (Lakatos et al, 2008;Stefanics et al, 2010;Lakatos et al, 2013;Henry and Herrmann, 2014;ten Oever et al, 2017), and is strongest in auditory cortex for low-frequency (<10 Hz) periodicities (Herrmann et al, 2013a;Keitel et al, 2017;Millman et al, 2017). Some studies report increased synchronization of neural activity with low-frequency amplitude modulations in sounds for older compared to younger humans (Purcell et al, 2004;Goossens et al, 2016;Presacco et al, 2016a) and non-human mammals (Overton and Recanzone, 2016;Herrmann et al, 2017;Lai et al, 2017;Parthasarathy et al, 2019).…”

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

“…Interestingly, whereas pure‐tone thresholds are by definition elevated in patients with sensorineural hearing loss, envelope detection thresholds are normal to better than normal (Füllgrabe, Meyer, & Lorenzi, ; Moore & Glasberg, ). Enhanced envelope coding is also evident in cortical EEG waves of people with sensorineural hearing loss and negatively correlates with speech identification in modulated noise (Millman, Mattys, Gouws, & Prendergast, ). Animal studies confirmed this finding by showing that temporal coding of the envelope, measured in single‐unit auditory nerve fibers and in auditory evoked potentials estimated to derive from the auditory midbrain, is similarly enhanced following noise‐induced hearing loss (Kale & Heinz, ; Zhong, Henry, & Heinz, ).…”