Impaired Sensory-motor Reconfiguration and Pupil-linked Arousal in Aging

Abstract

Mounting evidence indicates impairments of decision-making and brainstem arousal systems in aging. To shed light on the relationship between these phenomena, we compared behavior and dynamics of pupil-linked arousal between older and younger adults during compositionally structured tasks. The main task required continuous online inference about hidden changes in the stimulus-response mappings required for reporting a perceptual categorization judgment. Accuracy in that task was reduced in older compared to younger adults, impairment specifically reflecting objective and subjective difficulty in switching between stimulus-response mappings: there was no age difference in tasks requiring only the online inference or only the perceptual categorization under stable stimulus-response mappings. Participant[s] pupils reliably dilated during the categorization judgment as well as moments of high probability of switches in the online inference process in both age groups. But only when the switches prompted a change in stimulus-response association in the main task, were these pupil responses deteriorated in older compared to younger adults. We propose that impaired cognitive engagement of arousal in aging might limit the sensory-motor reconfigurations required for behavioral flexibility. SIGNIFICANCE STATEMENTAging affects decision-making, but the computational and physiological basis of these alterations are poorly understood. Here, we show that older people are impaired in switching the association between sensation and action to support flexible decision-making. This flexible switching process recruits pupil-linked arousal systems of the brainstem in a manner that is altered in older compared to younger individuals. By contrast, we find that several other computational processes required for complex decision-making, including rapid online inference about uncertain environments, and the associated pupil-linked arousal responses, are largely unaffected in older people. Our findings implicate an aberrant cognitive recruitment of brainstem arousal systems in age-related problems in decision-making.