An effect of dopamine depletion on decision-making: the temporal coupling of deliberation and execution

When a decision between alternative actions has to be made, the primate brain is able to uncouple motor execution from mental deliberation, providing time for higher cognitive processes such as remembering and reasoning. The mental deliberation leading to the decision and the motor execution applying the decision are likely to involve different neuronal circuits linking the basal ganglia and the frontal cortex. Behavioral and physiological studies in monkeys indicate that dopamine depletion may result in a loss of functional segregation between these circuits, hence, in interference between the deliberation and execution processes. To test this hypothesis in humans, we analyzed the movements of parkinsonian patients in a go/no-go task, contrasting periods of uncertainty with periods of knowledge about the rule to be applied. Two groups of patients were compared to healthy subjects: one group was treated with dopaminergic medication and the other with deep brain stimulation; both groups were also tested without any treatment. In healthy subjects, the movement time was unaffected by uncertainty. In untreated patients, the movement time increased with uncertainty, reflecting interference between deliberation and execution processes. This interference was fully corrected with dopaminergic medication but was unchanged with deep brain stimulation. Moreover, decision-related hesitations were detectable in the movements of dopamine-depleted patients, revealing a temporal coupling of deliberation and execution. We suggest that such coupling may be related to the loss of dopamine-mediated functional segregation between basal ganglia circuits processing different stages of goal-directed behavior.