Arousal state fluctuations destabilize speech intelligibility in older adults

Understanding speech in noisy, multi-talker environments is fundamental for social communication but becomes increasingly challenging as we age. Age-related hearing loss reduces audibility and degrades speech encoding, yet these deficits do not fully explain the momentary lapses in speech understanding that frustrate real-time communication. Here, we tested whether brain state fluctuations immediately before speech onset predict forthcoming speech recognition errors in older listeners. We measured the accuracy, speed, and consistency of speech recognition in 183 adults aged 18-76 years (103 female) using a brief, trial-based multi-talker listening task while tracking pupil dynamics before and during speech presentation. Prestimulus pupil-linked arousal predicted trial-level speech recognition in older, but not younger, adults, independent of hearing status, cognitive load, and task accuracy. In adults over 50 years of age, lower and higher extremes of prestimulus pupil size were associated with less accurate and slower responses, producing a striking inverted-U relationship between prestimulus arousal and forthcoming behavioral performance. Older adults exhibited lower extremes of pupil-linked arousal that were specifically associated with greater self-reported difficulty listening in everyday life. By contrast, stimulus-evoked pupil dilation during speech encoding, a measure of listening effort, did not predict trial-level performance at any age. These findings identify prestimulus pupil-linked arousal as a hidden marker of forthcoming lapses in speech intelligibility in older adults. When considered alongside conventional measures of peripheral hearing status in mixed-effects regression models, these measures provide a more complete accounting of biological changes underlying speech intelligibility deficits that frustrate social communication in older adults . Significance statement As we age, following a conversation in crowded environments becomes more difficult and frustrating, even when hearing tests appear normal. This study shows that fluctuations in arousal level (measured through prestimulus pupil size) are tightly linked to fluctuations in the speed and accuracy of speech processing in adults over 50 years of age. Changes in arousal state regulation uniquely accounted for the moment-to-moment variations in speech intelligibility and were more closely associated with self-reported listening challenges than other conventional measures. These findings highlight the contribution of brain-wide arousal systems to real-world listening challenges and identify a straightforward measure that could be used to more comprehensively assess and potentially improve speech understanding in social settings.