Altered orbitofrontal cortex neural variability underlies idiosyncratic experiences during aging

Abstract

Moment-to-moment neural variability plays a crucial role in learning and behavioral flexibility. Changes in this variability have been linked to age-associated differences in both task performances and resting-state activity. However, the effect of neural variability on specific computations and subjective experience remain unclear. Here, we demonstrate that changes to cortical neural variability during naturalistic experience serves as a readout of changes to region-specific computations, distinct from resting-state variability and mean neural activity. During affective experience, older adults exhibited an increase in neural variability within the orbitofrontal cortex (OFC). By employing a Bayesian learning model, we revealed that this corresponded to heightened uncertainty in the computational estimates of evolving valence in older adults. This model prediction was observed neurally with frequent state switching and temporally distorted representations within the OFC in older adults, compared to stable representations in the young. Crucially, these representational changes mirrored the arousal responses of the two groups. These results advance our understanding of how neural variability might carry unique information in aging, particularly to their changing and possibly idiosyncratic affective experiences.