Human choice strategy varies with anatomical projections from ventromedial prefrontal cortex to medial striatum

Abstract

Two distinct systems, goal-directed and habitual, support decision making. It has recently been hypothesized that this distinction may arise from two computational mechanisms, model-based and model-free reinforcement learning, neuronally implemented in frontostriatal circuits involved in learning and behavioral control. Here, we test whether the relative strength of anatomical connectivity within frontostriatal circuits accounts for variation in human individuals' reliance on model-based and model-free control. This hypothesis was tested by combining diffusion tensor imaging with a multistep decision task known to distinguish model-based and model-free control in humans. We found large interindividual differences in the degree of model-based control, and those differences are predicted by the structural integrity of white-matter tracts from the ventromedial prefrontal cortex to the medial striatum. Furthermore, an analysis based on masking out of bottom-up tracts suggests that this effect is driven by top-down influences from ventromedial prefrontal cortex to medial striatum. Our findings indicate that individuals with stronger afferences from the ventromedial prefrontal cortex to the medial striatum are more likely to rely on a model-based strategy to control their instrumental actions. These findings suggest a mechanism for instrumental action control through which medial striatum determines, at least partly, the relative contribution of model-based and model-free systems during decision-making according to top-down model-based information from the ventromedial prefrontal cortex. These findings have important implications for understanding the neural circuitry that might be susceptible to pathological computational processes in impulsive/compulsive psychiatric disorders. SIGNIFICANCE STATEMENT: Scholars from several disciplines have long been interested in the neural mechanisms of decision-making. An influential suggestion has structured decision-making into a flexible but expensive model-based system, and a more rapid but also more rigid model-free system. Here, we show that anatomical properties of the connections between frontal and striatal regions predict the use of a model-based system when individuals make decisions. Individuals with stronger top-down connectivity from the ventromedial prefrontal cortex to the medial striatum were more likely to rely on a model-based strategy during decision-making, suggesting that the ventromedial prefrontal cortex biases a striatal balance between model-based and model-free control. These findings qualify the neural implementation of decision-making computations and open the way for understanding decision-making pathologies.