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Preserved neural distinctiveness of speech in middle age despite cochlear neural degeneration: evidence from a gerbil model
Poster Session E, Sunday, September 14, 11:00 am - 12:30 pm, Field House
Zhe-chen Guo1, Aravindakshan Parthasarathy2, Bharath Chandrasekaran1; 1Northwestern University, 2University of Pittsburgh
Speech processing declines in middle age despite normal audiometric thresholds. Using electroencephalography (EEG) to continuous naturalistic speech, Guo et al. (2025) demonstrated that middle-aged adults exhibit less distinct neural representations of phonemes compared to younger adults, consistent with cortical neural dedifferentiation. This dedifferentiation were not fully explained by age-related cochlear neural degeneration (CND) as peripheral measures – including markers of putative CND – accounted for less than 30% of the variance. However, CND cannot be directly verified in vivo in humans, and hence the mechanisms underlying neural dedifferentiation with age remain unclear. Here, we establish the Mongolian gerbil – an rodent with hearing sensitivities similar to humans in the speech frequencies – as an animal model to study the mechanisms underlying neural dedifferentiation with age. We examine whether middle-aged Mongolian gerbils exhibit reduced neural representations of phonemes when exposed to naturalistic speech, and independently model peripheral changes and central plasticity to understand the causes behind neural dedifferentiation with age. Thirteen younger gerbils aged 18–40 weeks and sixteen middle-aged gerbils aged 75 weeks were used. Neural responses were recorded with subdermal electrodes placed on the animals’ scalp. Animals were presented with speech stimuli from the Alice’s Adventures in Wonderland audiobook at suprathreshold sound levels. To assess cochlear synaptopathy, immunohistological analysis of organ of Corti whole mounts was conducted to quantify average afferent synapse counts in the 1 kHz and 3 kHz cochlear regions. Neural data were analyzed following the phoneme-related potential (PRP) approach (Khalighinejad et al., 2017; Guo et al., 2025), whereby we epoched responses at the vertex electrode from 0.0–0.5 s to instances of each phoneme and averaged across instances to derive the PRP. We quantified neural distinctiveness of major speech categories (vowels, nasals/approximants, fricatives, and stops) by computing the F-statistic over time, which measures the variation in PRPs between categories relative to that within each category. Histological analysis revealed a ~20% reduction in afferent synapse counts in middle-aged gerbils compared with younger ones, consistent with age-related CND. Yet, the two age-groups did not differ significantly in the time-averaged F-statistic (t(24.43) = 0.30, p = 0.77) and the peak F value (t(26.87) = –0.48, p = 0.63). Across all animals, there was also no significant correlation between synapse count and time-averaged F-statistics (r = 0.25, p = 0.25). These findings from the animal model indicated that, unlike the middle-aged adults in Guo et al. (2025), middle-aged gerbils show no decline in neural distinctiveness of phoneme representations despite verified CND. This dissociation implies that cortical dedifferentiation of speech may not arise completely from reduced CND cascading downstream to the central auditory system. Ongoing analysis is aimed at modeling more extreme peripheral degradations using noise exposure, and independent maladaptive central plasticity using earplugs, to isolate the causes underlying neural dedifferentiation with age.
Topic Areas: Speech Perception,