
==== Front
bioRxiv
BIORXIV
bioRxiv
2692-8205
Cold Spring Harbor Laboratory

10.1101/2024.08.28.609778
preprint
1
Article
Reduced neural distinctiveness of speech representations in the middle-aged brain
Guo Zhe-chen http://orcid.org/0000-0003-0870-8321

McHaney Jacie R. http://orcid.org/0000-0002-1148-4018

Parthasarathy Aravindakshan http://orcid.org/0000-0002-4573-8004

Chandrasekaran Bharath http://orcid.org/0000-0002-3673-9435

30 8 2024
2024.08.28.609778https://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License, which allows reusers to distribute, remix, adapt, and build upon the material in any medium or format, so long as attribution is given to the creator. The license allows for commercial use.
http://biorxiv.org/lookup/doi/10.1101/2024.08.28.609778
nihpp-2024.08.28.609778.pdf
Abstract

Speech perception declines independent of hearing thresholds in middle-age, and the neurobiological reasons are unclear. In line with the age-related neural dedifferentiation hypothesis, we predicted that middle-aged adults show less distinct cortical representations of phonemes and acoustic-phonetic features relative to younger adults. In addition to an extensive audiological, auditory electrophysiological, and speech perceptual test battery, we measured electroencephalographic responses time-locked to phoneme instances (phoneme-related potential; PRP) in naturalistic, continuous speech and trained neural network classifiers to predict phonemes from these responses. Consistent with age-related neural dedifferentiation, phoneme predictions were less accurate, more uncertain, and involved a broader network for middle-aged adults compared with younger adults. Representational similarity analysis revealed that the featural relationship between phonemes was less robust in middle-age. Electrophysiological and behavioral measures revealed signatures of cochlear neural degeneration (CND) and speech perceptual deficits in middle-aged adults relative to younger adults. Consistent with prior work in animal models, signatures of CND were associated with greater cortical dedifferentiation, explaining nearly a third of the variance in PRP prediction accuracy together with measures of acoustic neural processing. Notably, even after controlling for CND signatures and acoustic processing abilities, age-group differences in PRP prediction accuracy remained. Overall, our results reveal “fuzzier” phonemic representations, suggesting that age-related cortical neural dedifferentiation can occur even in middle-age and may underlie speech perceptual challenges, despite a normal audiogram.
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