Neural correlates of impulse control behaviors in Parkinson's disease: Analysis of multimodal imaging data

Abstract

Background: Impulse control behaviors (ICB) are frequently observed in patients with Parkinson's disease (PD) and are characterized by compulsive and repetitive behavior resulting from the inability to resist internal drives.

Objectives: In this study, we aimed to provide a better understanding of structural and functional brain alterations and clinical parameters related to ICB in PD patients.

Methods: We utilized a dataset from the Parkinson's Progression Markers Initiative including 36 patients with ICB (PDICB+) compared to 76 without ICB (PDICB-) and 61 healthy controls (HC). Using multimodal MRI data we assessed gray matter brain volume, white matter integrity, and graph topological properties at rest.

Results: Compared with HC, PDICB+ showed reduced gray matter volume in the bilateral superior and middle temporal gyrus and in the right middle occipital gyrus. Compared with PDICB-, PDICB+ showed volume reduction in the left anterior insula. Depression and anxiety were more prevalent in PDICB+ than in PDICB- and HC. In PDICB+, lower gray matter volume in the precentral gyrus and medial frontal cortex, and higher axial diffusivity in the superior corona radiata were related to higher depression score. Both PD groups showed disrupted functional topological network pattern within the cingulate cortex compared with HC. PDICB+ vs PDICB- displayed reduced topological network pattern in the anterior cingulate cortex, insula, and nucleus accumbens.

Conclusions: Our results suggest that structural alterations in the insula and abnormal topological connectivity pattern in the salience network and the nucleus accumbens may lead to impaired decision making and hypersensitivity towards reward in PDICB+. Moreover, PDICB+ are more prone to suffer from depression and anxiety.

Keywords: Functional MRI; Impulse control behaviors; Parkinson’s disease; Structural magnetic resonance imaging (MRI).

Fig. 1

Significant gray matter volume loss in PDICB+ compared with HC (A) and PDICB+ compared with PDICB- (B). Results are shown at p < 0.05 Family-Wise Error (FWE) corrected using Threshold-Free Cluster Enhancement (TFCE) with age, total intracranial volume (TIV) and gender as covariates. L/R, left/right. Coordinates in MNI space; color bars represent P-values.

Fig. 2

Significant correlations of gray matter volume and white matter values (axial diffusivity) with the Geriatric Depression Scale (A and C) and trait anxiety (C). Scatter plots demonstrating the associations between regional volume loss (B) and Geriatric Depression Scale; (D) mean axial diffusivity and Geriatric Depression Scale and trait anxiety score (STAI). Results are shown at p < 0.05 Family-Wise Error (FWE) corrected using Threshold-Free Cluster Enhancement (TFCE) with age, total intracranial volume (TIV) and gender as covariates. L/R, left/right. Coordinates in MNI space; color bars represent P-values.

Fig. 3

Differences in functional topological network pattern between PDICB+ compared with PDICB- (A). Estimates from the Bayesian linear model shown in relation to HC = 0 (B). Error bars represent 95 % credible intervals. ACC sub, Anterior cingulate cortex subgenual; ACC pre, Anterior cingulate cortex pregenual; ACC sup, Anterior cingulate cortex supracallosal; MCC, middle cingulate and paracingulate gyri; N acc, Nucleus accumbens; VTA, Ventral tegmental area; ICB+, PD patients with ICB symptoms; ICB-, PD patients without ICB.