Dopamine-dependent reinforcement of motor skill learning: evidence from Gilles de la Tourette syndrome.

Abstract

Reinforcement learning theory has been extensively used to understand the neural underpinnings of instrumental behaviour. A central assumption surrounds dopamine signalling reward prediction errors, so as to update action values and ensure better choices in the future. However, educators may share the intuitive idea that reinforcements not only affect choices but also motor skills such as typing. Here, we employed a novel paradigm to demonstrate that monetary rewards can improve motor skill learning in humans. Indeed, healthy participants progressively got faster in executing sequences of key presses that were repeatedly rewarded with 10 euro compared with 1 cent. Control tests revealed that the effect of reinforcement on motor skill learning was independent of subjects being aware of sequence-reward associations. To account for this implicit effect, we developed an actor-critic model, in which reward prediction errors are used by the critic to update state values and by the actor to facilitate action execution. To assess the role of dopamine in such computations, we applied the same paradigm in patients with Gilles de la Tourette syndrome, who were either unmedicated or treated with neuroleptics. We also included patients with focal dystonia, as an example of hyperkinetic motor disorder unrelated to dopamine. Model fit showed the following dissociation: while motor skills were affected in all patient groups, reinforcement learning was selectively enhanced in unmedicated patients with Gilles de la Tourette syndrome and impaired by neuroleptics. These results support the hypothesis that overactive dopamine transmission leads to excessive reinforcement of motor sequences, which might explain the formation of tics in Gilles de la Tourette syndrome.

• Authors: Stefano Palminteri, Maël Lebreton, Yulia Worbe, Andreas Hartmann, Stéphane Lehéricy, Marie Vidailhet, David Grabli, Mathias Pessiglione
• Journal: Brain : a journal of neurology (Brain) Vol. 134 Issue Pt 8 Pg. 2287-301 (Aug 2011) ISSN: 1460-2156 [Electronic] England
• PMID: 21727098 (Publication Type: Journal Article, Research Support, Non-U.S. Gov't)

Chemical References

• Dopamine

Topics

• Adult
• Analysis of Variance
• Choice Behavior (physiology)
• Computer Simulation
• Dopamine (metabolism)
• Female
• Humans
• Learning (physiology)
• Male
• Models, Psychological
• Motor Skills Disorders (etiology)
• Reaction Time (physiology)
• Reinforcement, Psychology
• Tourette Syndrome (complications)
• Young Adult