A new theoretical framework jointly explains behavioral and neural variability across subjects performing flexible decision-making

Abstract

AbstractThe ability to flexibly select and accumulate relevant information to form decisions, while ignoring irrelevant information, is a fundamental component of higher cognition. Yet its neural mechanisms remain unclear. Here we demonstrate that, under assumptions supported by both monkey and rat data, the space of possible network mechanisms to implement this ability is spanned by the combination of three different components, each with specific behavioral and anatomical implications. We further show that existing electrophysiological and modeling data are compatible with the full variety of possible combinations of these components, suggesting that different individuals could use different component combinations. To study variations across subjects, we developed a rat task requiring context-dependent evidence accumulation, and trained many subjects on it. Our task delivers sensory evidence through pulses that have random but precisely known timing, providing high statistical power to characterize each individual’s neural and behavioral responses. Consistent with theoretical predictions, neural and behavioral analysis revealed remarkable heterogeneity across rats, despite uniformly good task performance. The theory further predicts a specific link between behavioral and neural signatures, which was robustly supported in the data. Our results provide a new experimentally-supported theoretical framework to analyze biological and artificial systems performing flexible decision-making tasks, and open the door to the study of individual variability in neural computations underlying higher cognition.