Low-dimensional factorized neural computations underlie risk-adaptive choices

Abstract

Real-world decision-making rarely occurs with perfect information. Instead, individuals must constantly weigh potential rewards against the probability of adverse outcomes.1 Failures of this process can lead to maladaptive decisions associated with reduced lifetime success, and numerous psychiatric disorders such as gambling addictions, bulimia nervosa, and substance use disorder.2,3 The neural computations that facilitate inference about the landscape of potential outcomes remain unclear, but are thought to occur in distributed frontotemporal circuits.4 Here we used deep reinforcement learning agents to predict distinct behavioral strategies and their underlying neural population dynamics during a risky decision-making task. Across a range of training conditions, deep reinforcement learning agents separated into strategies marked by either overly cautious exploration of the reward contingency space or a high-performing, risk-adaptive Bimodal strategy. The internal dynamics of high-performing Bimodal agents formed low-dimensional representations that segregated safe and risky states. In contrast, the cautious exploration agents were associated with more skewed and entangled neural representations. We found remarkably similar dynamical representations and their associated behavioral strategies in neuronal ensemble recordings from human epilepsy patients performing a similar risky decision-making task. These results reveal the structure of dynamical computations that underlie inferences about uncertain outcomes and their associated behavioral strategies.