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Endogenous fluctuations in the dopaminergic midbrain drive behavioral choice variability

Benjamin Chew,T. Hauser,M. Papoutsi,Joerg Magerkurth,R. Dolan,Robb B. Rutledge

Published 2019 in Proceedings of the National Academy of Sciences of the United States of America

ABSTRACT

Significance Humans are surprisingly inconsistent in their behavior, often making different choices under identical conditions. Previous research suggests that intrinsic fluctuations in brain activity can influence low-level processes, such as the amount of force applied in a motor response. Here, we show that intrinsic prestimulus brain activity in the dopaminergic midbrain influences how we choose between risky and safe options. Using computational modeling, we demonstrate that endogenous fluctuations alter phasic responses in a decision network and thereby modulate risk taking. Our findings demonstrate that higher-order cognition is influenced by fluctuations in internal brain states, providing a physiological basis for variability in complex human behavior. Human behavior is surprisingly variable, even when facing the same problem under identical circumstances. A prominent example is risky decision making. Economic theories struggle to explain why humans are so inconsistent. Resting-state studies suggest that ongoing endogenous fluctuations in brain activity can influence low-level perceptual and motor processes, but it remains unknown whether endogenous fluctuations also influence high-level cognitive processes including decision making. Here, using real-time functional magnetic resonance imaging, we tested whether risky decision making is influenced by endogenous fluctuations in blood oxygenation level-dependent (BOLD) activity in the dopaminergic midbrain, encompassing ventral tegmental area and substantia nigra. We show that low prestimulus brain activity leads to increased risky choice in humans. Using computational modeling, we show that increased risk taking is explained by enhanced phasic responses to offers in a decision network. Our findings demonstrate that endogenous brain activity provides a physiological basis for variability in complex human behavior.

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