Effects of Age on Brainstem Coding of Speech Glimpses in Interrupted Noise

Speech communication in background noise is particularly difficult for older adults—even those with normal hearing thresholds. Poor speech recognition is thought to be a consequence of age-related declines in temporal resolution (Frisina and Frisina, 1997; Gordon-Salant and Fitzgibbons, 1993), as well as declines in cognition and other higher-level processes (Akeroyd, 2008; Humes et al., 2012). Poor temporal resolution may impair speech recognition by limiting the listener's ability to use brief cues in speech, which are particularly important in fluctuating noise. In fluctuating backgrounds, listeners reconstruct partially masked messages based on brief moments when the signal-to-noise ratio (SNR) is favorable (Cooke, 2006; Best et al., 2017). This perceptual ability, known as “glimpsing,” is more difficult for older adults, even those with minimal hearing loss (Bologna et al., 2018). The purpose of this study was to test the hypothesis that age-related declines in temporal resolution reduce the neural fidelity (as determined by measures of brainstem coding) of speech cues during brief moments with favorable SNR.

Forward masking—the reduced detectability of an acoustic signal occurring after the offset of a masker—may explain the relationship between poor temporal resolution and the age-related decline in glimpsing. Dubno et al. (2003) measured detection thresholds for tonal signals occurring after the offset of a masker (forward-masked thresholds) as well as speech recognition in interrupted noise (a common paradigm for studying glimpsing) in the same sample of participants. They observed negative correlations between forward-masked thresholds and “masking release;” adults with poorer forward-masked thresholds received less benefit on the speech-recognition task when interruptions in the noise created momentary improvements in SNR. These results were interpreted in terms of the “recovery from prior stimulation” that is common to both the forward-masking and speech-recognition tasks. Masking release was dependent on the recovery of the response to a suprathreshold signal (tone or speech) following prior stimulation by a masker (Dubno et al., 2003). The strength of the association increased at higher rates of interruption, suggesting that forward masking from the preceding noise bursts was more disruptive to the recognition of shorter glimpses of speech. Similar results were reported by Fogerty et al. (2017), showing that older adults require longer durations after the offset of a masker to recognize consonant-vowel signals than younger adults. Physiological evidence that shorter glimpses are more susceptible to forward masking, particularly in older adults, would strengthen this theoretical relationship between forward masking, glimpsing, and age. Given that many older adults report difficulty understanding speech in noise despite relatively normal auditory thresholds (Beck et al., 2018), the ability to measure the underlying mechanism driving this relationship would offer considerable diagnostic utility.

Electrophysiological studies in humans and animals have provided insight into the potential mechanisms leading to the observed effects of age on glimpsing and forward masking. Animal models of aging suggest that neural activity in the brainstem becomes less temporally precise in older animals, even in the absence of peripheral hearing loss (Willott et al., 1988; Caspary et al., 1990). Precise neural firing allows the auditory system to capture fast changes in an acoustic environment, such as a momentary dip in the level of the background noise that would provide a glimpse of the speech signal. Electrophysiological work with human subjects has linked the age-related decline in temporal resolution to poor brainstem coding of speech and speech-like signals (Anderson et al., 2012; Clinard and Tremblay, 2013; Mamo et al., 2016; Parthasarathy et al., 2018; Vander Werff and Burns, 2011). These studies recorded auditory evoked potentials from younger and older adults in response to speech-like stimuli in quiet or with various maskers. Stimulus-locked responses can be processed to extract either the envelope or fine-structure component of the neural signal. These two components of the response, known as the envelope following response (EFR) and the frequency following response (FFR), respectively, reflect the neural representation of the acoustic envelope or fine structure of the evoking stimulus (Aiken and Picton, 2008). These techniques allow for quantitative measurement of the fidelity of brainstem coding (or at least certain aspects of it) in humans. Several independent groups have demonstrated that increasing age, poorer peripheral hearing sensitivity, or a combination of the two is associated with poorer fidelity of the EFR and FFR, particularly in noise (Hao et al., 2018; McClasky et al., 2019; Schoof and Rosen, 2016). The current study used the EFR to investigate the extent to which physiological declines in brainstem coding may explain effects of age on glimpsing and forward masking of speech glimpses.

In this study, EFRs to glimpses of speech-like stimuli interrupted by silence or noise were elicited from adults spanning a wide range of ages. The effect of glimpse duration was evaluated with stimuli consisting of either a single long glimpse, three medium glimpses, or five short glimpses, with equivalent stimulus energy across the three conditions. The effect of forward masking on the EFR was determined by comparing responses to glimpses interrupted by silence to glimpses interrupted by non-simultaneous masking noise. We expected that older adults would demonstrate poorer overall EFR strength than younger adults, as seen in several previous studies (e.g., Anderson et al., 2012; Clinard and Tremblay, 2013; Vander Werff and Burns, 2011). We hypothesized that age-related declines in glimpsing were driven by poor brainstem coding of speech glimpses and predicted that older adults would demonstrate particularly poor responses to shorter glimpses of speech (i.e., interaction between age and glimpse duration, as seen in Bologna et al., 2018). We also hypothesized that poor brainstem coding contributed to prolonged susceptibility to forward masking in older adults and predicted that poor responses would be observed when glimpses were interrupted by noise compared to silence, particularly for older adults and with shorter glimpses of speech (as shown behaviorally in Dubno et al., 2003 and Fogerty et al., 2017). Evidence supporting these hypotheses would suggest that age-related declines in glimpsing may be driven by poor brainstem coding of speech glimpses.

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