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Mesocorticolimbic hemodynamic response in Parkinson's disease patients with compulsive behaviors.

ABSTRACT: BACKGROUND:PD patients treated with dopamine therapy can develop maladaptive impulsive and compulsive behaviors, manifesting as repetitive participation in reward-driven activities. This behavioral phenotype implicates aberrant mesocorticolimbic network function, a concept supported by past literature. However, no study has investigated the acute hemodynamic response to dopamine agonists in this subpopulation. OBJECTIVES:We tested the hypothesis that dopamine agonists differentially alter mesocortical and mesolimbic network activity in patients with impulsive-compulsive behaviors. METHODS:Dopamine agonist effects on neuronal metabolism were quantified using arterial-spin-labeling MRI measures of cerebral blood flow in the on-dopamine agonist and off-dopamine states. The within-subject design included 34 PD patients, 17 with active impulsive compulsive behavior symptoms, matched for age, sex, disease duration, and PD severity. RESULTS:Patients with impulsive-compulsive behaviors have a significant increase in ventral striatal cerebral blood flow in response to dopamine agonists. Across all patients, ventral striatal cerebral blood flow on-dopamine agonist is significantly correlated with impulsive-compulsive behavior severity (Questionnaire for Impulsive Compulsive Disorders in Parkinson's Disease- Rating Scale). Voxel-wise analysis of dopamine agonist-induced cerebral blood flow revealed group differences in mesocortical (ventromedial prefrontal cortex; insular cortex), mesolimbic (ventral striatum), and midbrain (SN; periaqueductal gray) regions. CONCLUSIONS:These results indicate that dopamine agonist therapy can augment mesocorticolimbic and striato-nigro-striatal network activity in patients susceptible to impulsive-compulsive behaviors. Our findings reinforce a wider literature linking studies of maladaptive behaviors to mesocorticolimbic networks and extend our understanding of biological mechanisms of impulsive compulsive behaviors in PD. © 2017 International Parkinson and Movement Disorder Society.

SUBMITTER: Claassen DO

PROVIDER: S-EPMC5681361 | biostudies-literature | 2017 Nov

REPOSITORIES: biostudies-literature

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Mesocorticolimbic hemodynamic response in Parkinson's disease patients with compulsive behaviors.

Claassen Daniel O DO Stark Adam J AJ Spears Charis A CA Petersen Kalen J KJ van Wouwe Nelleke C NC Kessler Robert M RM Zald David H DH Donahue Manus J MJ

Movement disorders : official journal of the Movement Disorder Society 20170619 11

<h4>Background</h4>PD patients treated with dopamine therapy can develop maladaptive impulsive and compulsive behaviors, manifesting as repetitive participation in reward-driven activities. This behavioral phenotype implicates aberrant mesocorticolimbic network function, a concept supported by past literature. However, no study has investigated the acute hemodynamic response to dopamine agonists in this subpopulation.<h4>Objectives</h4>We tested the hypothesis that dopamine agonists differential ...[more]

PMID: 28627133

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Project description:BackgroundImpulsive compulsive behaviors (ICBs) often disturb patients with Parkinson's Disease (PD), of which impulse control disorder (ICD) and dopamine dysregulation syndrome (DDS) are two major subsets. The nucleus accumbens (NAcc) is involved in ICB; however, it remains unclear how the NAcc affects cortical function and defines the different behavioral characteristics of ICD and DDS.ObjectivesTo identify the cortico-striatal network primarily involved in ICB and the differences in these networks between patients with ICD and DDS using structural and resting-state functional magnetic resonance imaging.MethodsPatients with PD were recruited using data from a previous cohort study and divided into those with ICB (ICB group) and without ICB (non-ICB group) using the Japanese version of the Questionnaire for Impulsive Compulsive Disorders in Parkinson's Disease (J-QUIP). From these two groups, we extracted 37 pairs matched for age, sex, disease duration, and levodopa equivalent daily dose of dopamine agonists. Patients with ICB were further classified as having ICD or DDS based on the J-QUIP subscore. General linear models were used to compare gray matter volume and functional connectivity (FC) of the NAcc, caudate, and putamen between the ICB and non-ICB groups and between patients with ICD and those with DDS.ResultsWe found no significant differences in gray matter volumebetween the ICB and non-ICB groups or between patients with ICD and those with DDS. Compared with the non-ICB group, the FC of the right NAcc in the ICB group was lower in the bilateral ventromedial prefrontal cortex and higher in the left middle occipital gyrus. Furthermore, patients with DDS showed higher FC between the right putamen and left superior temporal gyrus and higher FC between the left caudate and bilateral middle occipital gyrus than patients with ICD. In contrast, patients with ICD exhibited higher FC between the left NAcc and the right posterior cingulate cortex than patients with DDS.ConclusionsThe functionally altered network between the right NAcc and ventromedial prefrontal cortex was associated with ICB in PD. In addition, the surrounding cortico-striatal networks may differentiate the behavioral characteristics of patients with ICD and those with DDS.

Dataset Information

Mesocorticolimbic hemodynamic response in Parkinson's disease patients with compulsive behaviors.

Publications

Mesocorticolimbic hemodynamic response in Parkinson's disease patients with compulsive behaviors.

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