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Recent work has identified a critical role for the hippocampus in reward‐sensitive behaviors, including motivated memory, reinforcement learning, and decision‐making. Animal histology and human functional neuroimaging have shown that brain regions involved in reward processing and motivation are more interconnected with the ventral/anterior hippocampus. However, direct evidence examining gradients of structural connectivity between reward regions and the hippocampus in humans is lacking. The present study used diffusion MRI (dMRI) and probabilistic tractography to quantify the structural connectivity of the hippocampus with key reward processing regions in vivo. Using a large sample of subjects (N = 628) from the human connectome dMRI data release, we found that connectivity profiles with the hippocampus varied widely between different regions of the reward circuit. While the dopaminergic midbrain (ventral tegmental area) showed stronger connectivity with the anterior versus posterior hippocampus, the ventromedial prefrontal cortex showed stronger connectivity with the posterior hippocampus. The limbic (ventral) striatum demonstrated a more homogeneous connectivity profile along the hippocampal long axis. This is the first study to generate a probabilistic atlas of the hippocampal structural connectivity with reward‐related networks, which is essential to investigating how these circuits contribute to normative adaptive behavior and maladaptive behaviors in psychiatric illness. These findings describe nuanced structural connectivity that sets the foundation to better understand how the hippocampus influences reward‐guided behavior in humans. [ABSTRACT FROM AUTHOR]

Both goal-directed and automatic processes shape human behavior, but these processes often conflict. Behavioral control is the decision about which process guides behavior. Despite the importance of behavioral control for adaptive decision-making, its neural mechanisms remain unclear. Critically, it is unknown if there are mechanisms for behavioral control that are distinct from those supporting the formation of goal-relevant knowledge. We performed deep phenotyping of individual dopamine system function by combining multiple PET scans, fMRI, and dopaminergic drug administration in a within-subject, double-blind, placebo-controlled design. Subjects performed a rule-based response time task, with goal-directed and automatic decision-making operationalized as model-based and model-free influences on behavior. We found a double dissociation between two aspects of ventral striatal dopamine physiology: D2/3 receptor availability and dopamine synthesis capacity. Convergent and causal evidence indicated that D2/3 receptors regulate behavioral control by enhancing model-based and blunting model-free influences on behavior but do not affect model-based knowledge formation. In contrast, dopamine synthesis capacity was linked to the formation of model-based knowledge but not behavioral control. D2/3 receptors also modulated frontostriatal functional connectivity, suggesting they regulate behavioral control by gating prefrontal inputs to the striatum. These results identify central mechanisms underlying individual and state differences in behavioral control and point to striatal D2/3 receptors as targets for interventions for improving goal-directed behavior.

Stimulus-response habits benefit behavior by automatizing the selection of rewarding actions. However, this automaticity can come at the cost of reduced flexibility to adapt behavior when circumstances change. The goal-directed system is thought to counteract the habit system by providing the flexibility to pursue context-appropriate behaviors. The dichotomy between habitual action selection and flexible goal-directed behavior has recently been challenged by findings showing that rewards bias both action and goal selection. Here, we test whether reward reinforcement can give rise to habitual goal selection much as it gives rise to habitual action selection. We designed a rewarded, context-based perceptual discrimination task in which performance on one rule was reinforced. Using drift-diffusion models and psychometric analyses, we found that reward facilitates the initiation and execution of rules. Strikingly, we found that these biases persisted in a test phase in which rewards were no longer available. Although this facilitation is consistent with the habitual goal selection hypothesis, we did not find evidence that reward reinforcement reduced cognitive flexibility to implement alternative rules. Together, the findings suggest that reward creates a lasting impact on the selection and execution of goals but may not lead to the inflexibility characteristic of habits. Our findings demonstrate the role of the reward learning system in influencing how the goal-directed system selects and implements goals., (© 2024 Massachusetts Institute of Technology.)