Abstract
Realtime modulation of brainstem frequency-following responses (FFRs) by online changes in cortical arousal state via the corticofugal (top-down) pathway has been demonstrated previously in younger humans and is more prominent in the presence of background noise. FFRs during high cortical arousal states also have a stronger relationship with speech behaviors. Aging is associated with overexaggerated auditory responses, which might reflect degraded inhibitory processing within the peripheral and ascending pathways, or changes in attentional control regulation via descending auditory pathways. Here, we tested the hypothesis that online corticofugal interplay is impacted in age-related hearing loss. We measured EEG in older adults with normal-hearing (NH) and hearing-loss (HL) while they actively performed speech identification tasks in different noise backgrounds. We measured α power to index online arousal states during task engagement and separate speech-FFRs according to fluctuations in cortical activity. We found cortical α power was smaller in the HL than NH group. In NH listeners, α-FFRs modulation for clear speech also resembled that previously observed in noise among younger adults. Cortical-brainstem modulation was further diminished by noise and with HL in older adults. Lastly, neural decoding showed low-α FFRs were more predictive of behavioral measures and carried more stimulus-related information of speech in NH individuals. Our findings provide evidence that age-related hearing loss affects cortical-brainstem interplay in the auditory system. Aberrant modulation of brainstem speech processing exposes a new underlying mechanism for the listening difficulties faced by older adults when engaging in cocktail party-like conversations.
Significant Statement Top-down (e.g., attention and arousal) effects on human brainstem responses have been controversial. Here, we show that cortical activity (indexed by EEG α-band amplitudes) is associated with trial-by-trial changes in brainstem speech representations measured via frequency-following responses. More critically, we show these cortical-subcortical interactions are particularly prominent during active speech listening tasks in normal-hearing older adults and differentially changed in older adults with hearing loss. Our study reveals cortical arousal state actively shapes brainstem speech representations and provide a potential new mechanism for older listeners’ difficulties perceiving speech in cocktail party-like listening situations in the form of a miss-coordination between cortical and subcortical levels of auditory processing.
Competing Interest Statement
The authors have declared no competing interest.