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Impulse control disorder in Parkinson’s disease is associated with abnormal frontal value signalling
Dopaminergic medication is well established to boost reward- versus punishment-based learning in Parkinson’s disease. However, there is tremendous variability in dopaminergic medication effects across different individuals, with some patients exhibiting much greater cognitive sensitivity to medicati...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10473575/ https://www.ncbi.nlm.nih.gov/pubmed/37192341 http://dx.doi.org/10.1093/brain/awad162 |
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author | Tichelaar, Jorryt G Sayalı, Ceyda Helmich, Rick C Cools, Roshan |
author_facet | Tichelaar, Jorryt G Sayalı, Ceyda Helmich, Rick C Cools, Roshan |
author_sort | Tichelaar, Jorryt G |
collection | PubMed |
description | Dopaminergic medication is well established to boost reward- versus punishment-based learning in Parkinson’s disease. However, there is tremendous variability in dopaminergic medication effects across different individuals, with some patients exhibiting much greater cognitive sensitivity to medication than others. We aimed to unravel the mechanisms underlying this individual variability in a large heterogeneous sample of early-stage patients with Parkinson’s disease as a function of comorbid neuropsychiatric symptomatology, in particular impulse control disorders and depression. One hundred and ninety-nine patients with Parkinson’s disease (138 ON medication and 61 OFF medication) and 59 healthy controls were scanned with functional MRI while they performed an established probabilistic instrumental learning task. Reinforcement learning model-based analyses revealed medication group differences in learning from gains versus losses, but only in patients with impulse control disorders. Furthermore, expected-value related brain signalling in the ventromedial prefrontal cortex was increased in patients with impulse control disorders ON medication compared with those OFF medication, while striatal reward prediction error signalling remained unaltered. These data substantiate the hypothesis that dopamine’s effects on reinforcement learning in Parkinson’s disease vary with individual differences in comorbid impulse control disorder and suggest they reflect deficient computation of value in medial frontal cortex, rather than deficient reward prediction error signalling in striatum. See Michael Browning (https://doi.org/10.1093/brain/awad248) for a scientific commentary on this article. |
format | Online Article Text |
id | pubmed-10473575 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-104735752023-09-02 Impulse control disorder in Parkinson’s disease is associated with abnormal frontal value signalling Tichelaar, Jorryt G Sayalı, Ceyda Helmich, Rick C Cools, Roshan Brain Original Article Dopaminergic medication is well established to boost reward- versus punishment-based learning in Parkinson’s disease. However, there is tremendous variability in dopaminergic medication effects across different individuals, with some patients exhibiting much greater cognitive sensitivity to medication than others. We aimed to unravel the mechanisms underlying this individual variability in a large heterogeneous sample of early-stage patients with Parkinson’s disease as a function of comorbid neuropsychiatric symptomatology, in particular impulse control disorders and depression. One hundred and ninety-nine patients with Parkinson’s disease (138 ON medication and 61 OFF medication) and 59 healthy controls were scanned with functional MRI while they performed an established probabilistic instrumental learning task. Reinforcement learning model-based analyses revealed medication group differences in learning from gains versus losses, but only in patients with impulse control disorders. Furthermore, expected-value related brain signalling in the ventromedial prefrontal cortex was increased in patients with impulse control disorders ON medication compared with those OFF medication, while striatal reward prediction error signalling remained unaltered. These data substantiate the hypothesis that dopamine’s effects on reinforcement learning in Parkinson’s disease vary with individual differences in comorbid impulse control disorder and suggest they reflect deficient computation of value in medial frontal cortex, rather than deficient reward prediction error signalling in striatum. See Michael Browning (https://doi.org/10.1093/brain/awad248) for a scientific commentary on this article. Oxford University Press 2023-05-16 /pmc/articles/PMC10473575/ /pubmed/37192341 http://dx.doi.org/10.1093/brain/awad162 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of the Guarantors of Brain. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com |
spellingShingle | Original Article Tichelaar, Jorryt G Sayalı, Ceyda Helmich, Rick C Cools, Roshan Impulse control disorder in Parkinson’s disease is associated with abnormal frontal value signalling |
title | Impulse control disorder in Parkinson’s disease is associated with abnormal frontal value signalling |
title_full | Impulse control disorder in Parkinson’s disease is associated with abnormal frontal value signalling |
title_fullStr | Impulse control disorder in Parkinson’s disease is associated with abnormal frontal value signalling |
title_full_unstemmed | Impulse control disorder in Parkinson’s disease is associated with abnormal frontal value signalling |
title_short | Impulse control disorder in Parkinson’s disease is associated with abnormal frontal value signalling |
title_sort | impulse control disorder in parkinson’s disease is associated with abnormal frontal value signalling |
topic | Original Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10473575/ https://www.ncbi.nlm.nih.gov/pubmed/37192341 http://dx.doi.org/10.1093/brain/awad162 |
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