Cortical and Striatal Reward Processing in Parkinson’s Disease Psychosis
Psychotic symptoms frequently occur in Parkinson’s disease (PD), but their pathophysiology is poorly understood. According to the National Institute of Health RDoc programme, the pathophysiological basis of neuropsychiatric symptoms may be better understood in terms of dysfunction of underlying doma...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2017-04-01
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| Series: | Frontiers in Neurology |
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| Online Access: | http://journal.frontiersin.org/article/10.3389/fneur.2017.00156/full |
| _version_ | 1818249619292815360 |
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| author | Graham K. Murray Graham K. Murray Graham K. Murray Graham K. Murray Sara Garofalo Sara Garofalo Azucena Justicia Gonzalo Arrondo Anna O. Ermakova Pranathi Ramachandra Carina Tudor-Sfetea Trevor W. Robbins Trevor W. Robbins Roger A. Barker Paul C. Fletcher Paul C. Fletcher Paul C. Fletcher |
| author_facet | Graham K. Murray Graham K. Murray Graham K. Murray Graham K. Murray Sara Garofalo Sara Garofalo Azucena Justicia Gonzalo Arrondo Anna O. Ermakova Pranathi Ramachandra Carina Tudor-Sfetea Trevor W. Robbins Trevor W. Robbins Roger A. Barker Paul C. Fletcher Paul C. Fletcher Paul C. Fletcher |
| author_sort | Graham K. Murray |
| collection | DOAJ |
| description | Psychotic symptoms frequently occur in Parkinson’s disease (PD), but their pathophysiology is poorly understood. According to the National Institute of Health RDoc programme, the pathophysiological basis of neuropsychiatric symptoms may be better understood in terms of dysfunction of underlying domains of neurocognition in a trans-diagnostic fashion. Abnormal cortico-striatal reward processing has been proposed as a key domain contributing to the pathogenesis of psychotic symptoms in schizophrenia. This theory has received empirical support in the study of schizophrenia spectrum disorders and preclinical models of psychosis, but has not been tested in the psychosis associated with PD. We, therefore, investigated brain responses associated with reward expectation and prediction error signaling during reinforcement learning in PD-associated psychosis. An instrumental learning task with monetary gains and losses was conducted during an fMRI study in PD patients with (n = 12), or without (n = 17), a history of psychotic symptoms, along with a sample of healthy controls (n = 24). We conducted region of interest analyses in the ventral striatum (VS), ventromedial prefrontal and posterior cingulate cortices, and whole-brain analyses. There was reduced activation in PD patients with a history of psychosis, compared to those without, in the posterior cingulate cortex and the VS during reward anticipation (p < 0.05 small volume corrected). The results suggest that cortical and striatal abnormalities in reward processing, a putative pathophysiological mechanism of psychosis in schizophrenia, may also contribute to the pathogenesis of psychotic symptoms in PD. The finding of posterior cingulate dysfunction is in keeping with prior results highlighting cortical dysfunction in the pathogenesis of PD psychosis. |
| first_indexed | 2024-12-12T15:39:22Z |
| format | Article |
| id | doaj.art-d6dd8447ee36417eaec230009922e7c0 |
| institution | Directory Open Access Journal |
| issn | 1664-2295 |
| language | English |
| last_indexed | 2024-12-12T15:39:22Z |
| publishDate | 2017-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neurology |
| spelling | doaj.art-d6dd8447ee36417eaec230009922e7c02022-12-22T00:19:56ZengFrontiers Media S.A.Frontiers in Neurology1664-22952017-04-01810.3389/fneur.2017.00156254012Cortical and Striatal Reward Processing in Parkinson’s Disease PsychosisGraham K. Murray0Graham K. Murray1Graham K. Murray2Graham K. Murray3Sara Garofalo4Sara Garofalo5Azucena Justicia6Gonzalo Arrondo7Anna O. Ermakova8Pranathi Ramachandra9Carina Tudor-Sfetea10Trevor W. Robbins11Trevor W. Robbins12Roger A. Barker13Paul C. Fletcher14Paul C. Fletcher15Paul C. Fletcher16Department of Psychiatry, University of Cambridge, Cambridge, UKBehavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, UKCambridgeshire and Peterborough NHS Foundation Trust, Cambridge, UKCambridge University Hospitals NHS Foundation Trust, Cambridge, UKDepartment of Psychiatry, University of Cambridge, Cambridge, UKBehavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, UKDepartment of Psychiatry, University of Cambridge, Cambridge, UKDepartment of Psychiatry, University of Cambridge, Cambridge, UKDepartment of Psychiatry, University of Cambridge, Cambridge, UKCambridgeshire and Peterborough NHS Foundation Trust, Cambridge, UKDepartment of Psychiatry, University of Cambridge, Cambridge, UKBehavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, UKDepartment of Psychology, University of Cambridge, Cambridge, UKDepartment of Clinical Neuroscience, University of Cambridge, Cambridge, UKDepartment of Psychiatry, University of Cambridge, Cambridge, UKCambridgeshire and Peterborough NHS Foundation Trust, Cambridge, UKCambridge University Hospitals NHS Foundation Trust, Cambridge, UKPsychotic symptoms frequently occur in Parkinson’s disease (PD), but their pathophysiology is poorly understood. According to the National Institute of Health RDoc programme, the pathophysiological basis of neuropsychiatric symptoms may be better understood in terms of dysfunction of underlying domains of neurocognition in a trans-diagnostic fashion. Abnormal cortico-striatal reward processing has been proposed as a key domain contributing to the pathogenesis of psychotic symptoms in schizophrenia. This theory has received empirical support in the study of schizophrenia spectrum disorders and preclinical models of psychosis, but has not been tested in the psychosis associated with PD. We, therefore, investigated brain responses associated with reward expectation and prediction error signaling during reinforcement learning in PD-associated psychosis. An instrumental learning task with monetary gains and losses was conducted during an fMRI study in PD patients with (n = 12), or without (n = 17), a history of psychotic symptoms, along with a sample of healthy controls (n = 24). We conducted region of interest analyses in the ventral striatum (VS), ventromedial prefrontal and posterior cingulate cortices, and whole-brain analyses. There was reduced activation in PD patients with a history of psychosis, compared to those without, in the posterior cingulate cortex and the VS during reward anticipation (p < 0.05 small volume corrected). The results suggest that cortical and striatal abnormalities in reward processing, a putative pathophysiological mechanism of psychosis in schizophrenia, may also contribute to the pathogenesis of psychotic symptoms in PD. The finding of posterior cingulate dysfunction is in keeping with prior results highlighting cortical dysfunction in the pathogenesis of PD psychosis.http://journal.frontiersin.org/article/10.3389/fneur.2017.00156/fullventral striatumposterior cingulate cortexprediction errorreinforcement learningfMRI |
| spellingShingle | Graham K. Murray Graham K. Murray Graham K. Murray Graham K. Murray Sara Garofalo Sara Garofalo Azucena Justicia Gonzalo Arrondo Anna O. Ermakova Pranathi Ramachandra Carina Tudor-Sfetea Trevor W. Robbins Trevor W. Robbins Roger A. Barker Paul C. Fletcher Paul C. Fletcher Paul C. Fletcher Cortical and Striatal Reward Processing in Parkinson’s Disease Psychosis Frontiers in Neurology ventral striatum posterior cingulate cortex prediction error reinforcement learning fMRI |
| title | Cortical and Striatal Reward Processing in Parkinson’s Disease Psychosis |
| title_full | Cortical and Striatal Reward Processing in Parkinson’s Disease Psychosis |
| title_fullStr | Cortical and Striatal Reward Processing in Parkinson’s Disease Psychosis |
| title_full_unstemmed | Cortical and Striatal Reward Processing in Parkinson’s Disease Psychosis |
| title_short | Cortical and Striatal Reward Processing in Parkinson’s Disease Psychosis |
| title_sort | cortical and striatal reward processing in parkinson s disease psychosis |
| topic | ventral striatum posterior cingulate cortex prediction error reinforcement learning fMRI |
| url | http://journal.frontiersin.org/article/10.3389/fneur.2017.00156/full |
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