Disruption of Dorsolateral Prefrontal Cortex Decreases Model-Based in Favor of Model-free Control in Humans

Smittenaar, Peter; FitzGerald, Thomas H. B.; Romei, Vincenzo; Wright, Nicholas D.; Dolan, Raymond J. · 2013 · OpenAlex-citations

DOI: 10.1016/j.neuron.2013.08.009

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Summary

This study investigates the causal role of the dorsolateral prefrontal cortex (dlPFC) in human decision-making, specifically addressing how the brain balances between "model-free" (habitual, computationally efficient) and "model-based" (flexible, goal-directed) control systems. While previous research suggested the dlPFC supports model-based processes, evidence was largely correlational. The authors aimed to provide causal evidence by manipulating the relative dominance of these control systems through transient disruption of the dlPFC. The researchers employed a within-subjects design with 25 participants who underwent three separate testing sessions. In each session, participants received MRI-guided theta burst transcranial magnetic stimulation (TBS) to either the right dlPFC, left dlPFC, or a control site (vertex). TBS induces temporary cortical inhibition. Participants then performed a two-stage decision-making task designed to dissociate model-free and model-based strategies. In this task, choices at the first stage probabilistically determined available options at the second stage, with one transition being more common (70%) than the other. Model-free agents repeat rewarded actions regardless of transition probability, whereas model-based agents use the transition structure to plan ahead, particularly switching choices after rewards following uncommon transitions. Behavioral data were analyzed using hierarchical logistic regression to quantify the influence of reward (model-free) and the interaction between reward and transition likelihood (model-based). The results demonstrated that disruption of the right dlPFC significantly reduced model-based control and shifted the behavioral balance toward model-free dominance compared to the vertex control. In contrast, disruption of the left dlPFC did not significantly impair model-based control in the general population. However, further analysis revealed that the effect of left dlPFC disruption depended on individual working memory (WM) capacity. Participants with low WM capacity showed impaired model-based control after left dlPFC disruption, whereas those with high WM capacity retained model-based performance. This suggests that the left dlPFC’s role in model-based control is contingent on baseline WM resources, potentially mediated by dopamine levels which covary with WM. These findings provide the first causal evidence in humans that the right dlPFC is a critical node for model-based, flexible decision-making. The study establishes that disrupting this region forces a reliance on less optimal, habitual control strategies. Furthermore, it highlights functional asymmetries within the prefrontal cortex, indicating that while the right dlPFC is essential for model-based control regardless of individual differences, the left dlPFC supports this process primarily in individuals with lower working memory capacity. This work clarifies the neural architecture underlying deliberative choice and offers insights into how disruptions in prefrontal function might contribute to disorders characterized by rigid, habitual behaviors.

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• executive function