Probabilistic classification learning with corrective feedback is associated with in vivo striatal dopamine release in the ventral striatum, while learning without feedback is not

• Published in: Human brain mapping 2014-10, Vol.35 (10), p.5106-5115
• Main Authors: Wilkinson, Leonora, Tai, Yen Foung, Lin, Chia Shu, Lagnado, David Albert, Brooks, David James, Piccini, Paola, Jahanshahi, Marjan
• Format: Article
• Language: English
• Subjects: 11C-raclopride positron emission tomography; Aged; Analysis of Variance; basal ganglia; Biological and medical sciences; Brain Mapping; Dopamine - metabolism; Dopamine Antagonists - metabolism; Feedback, Psychological - physiology; Female; Functional Laterality; Fundamental and applied biological sciences. Psychology; Human; Humans; Investigative techniques, diagnostic techniques (general aspects); Learning; Learning. Memory; Male; Medical sciences; Middle Aged; Nervous system; non-motor skill learning; Paired-Associate Learning - physiology; Positron-Emission Tomography; Predictive Value of Tests; probabilistic learning; Probability Learning; procedural learning; Protein Binding - drug effects; Psychology. Psychoanalysis. Psychiatry; Psychology. Psychophysiology; Raclopride - metabolism; Radiodiagnosis. Nmr imagery. Nmr spectrometry; Ventral Striatum - diagnostic imaging; Ventral Striatum - metabolism; weather prediction task
• ISSN: 1065-9471; 1097-0193
• DOI: 10.1002/hbm.22536

The basal ganglia (BG) mediate certain types of procedural learning, such as probabilistic classification learning on the ‘weather prediction task’ (WPT). Patients with Parkinson's disease (PD), who have BG dysfunction, are impaired at WPT‐learning, but it remains unclear what component of the WPT is important for learning to occur. We tested the hypothesis that learning through processing of corrective feedback is the essential component and is associated with release of striatal dopamine. We employed two WPT paradigms, either involving learning via processing of corrective feedback (FB) or in a paired associate manner (PA). To test the prediction that learning on the FB but not PA paradigm would be associated with dopamine release in the striatum, we used serial 11C‐raclopride (RAC) positron emission tomography (PET), to investigate striatal dopamine release during FB and PA WPT‐learning in healthy individuals. Two groups, FB, (n = 7) and PA (n = 8), underwent RAC PET twice, once while performing the WPT and once during a control task. Based on a region‐of‐interest approach, striatal RAC‐binding potentials reduced by 13–17% in the right ventral striatum when performing the FB compared to control task, indicating release of synaptic dopamine. In contrast, right ventral striatal RAC binding non‐significantly increased by 9% during the PA task. While differences between the FB and PA versions of the WPT in effort and decision‐making is also relevant, we conclude striatal dopamine is released during FB‐based WPT‐learning, implicating the striatum and its dopamine connections in mediating learning with FB. Hum Brain Mapp 35:5106–5115, 2014. © 2014 The Authors. Human Brain Mapping Published by Wiley Periodicals, Inc.