Cortical-brainstem interplay during speech perception in older adults with and without hearing loss

Introduction Real time 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 young adults and is more prominent in the presence of background noise. FFRs during high cortical arousal states also have a stronger relationship with speech perception. Aging is associated with increased auditory brain 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 by age-related hearing loss. Methods We measured EEG in older adults with normal-hearing (NH) and mild to moderate hearing-loss (HL) while they performed speech identification tasks in different noise backgrounds. We measured α power to index online cortical arousal states during task engagement. Subsequently, we split brainstem speech-FFRs, on a trial-by-trial basis, according to fluctuations in concomitant cortical α power into low or high α FFRs to index cortical-brainstem modulation. Results We found cortical α power was smaller in the HL than the NH group. In NH listeners, α-FFRs modulation for clear speech (i.e., without noise) also resembled that previously observed in younger adults for speech in noise. Cortical-brainstem modulation was further diminished in HL older adults in the clear condition and by noise in NH older adults. Machine learning classification showed low α FFR frequency spectra yielded higher accuracy for classifying listeners’ perceptual performance in both NH and HL participants. Moreover, low α FFRs decreased with increased hearing thresholds at 0.5–2 kHz for clear speech but noise generally reduced low α FFRs in the HL group. Discussion Collectively, our study reveals cortical arousal state actively shapes brainstem speech representations and provides 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.