Reduced neural distinctiveness of speech representations in the middle-aged brain

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.