Brain structural and functional signatures of impulsive–compulsive behaviours in Parkinson’s disease

Abstract

This study assessed brain structural and functional alterations in patients with Parkinson's disease and impulsive-compulsive behaviours (PD-ICB) compared with controls and PD no-ICB cases. Eighty-five PD patients (35 PD-ICB) and 50 controls were recruited. All subjects underwent three-dimensional T1-weighted, diffusion tensor (DT), and resting state functional magnetic resonance imaging (RS fMRI). We assessed cortical thickness with surface-based morphometry, subcortical volumes using FIRST, DT MRI metrics using region of interest and tractography approaches, and RS fMRI using a model free approach. Compared with controls, both PD groups showed a pattern of brain structural alterations in the basal ganglia (more evident in PD no-ICB patients), sensorimotor and associative systems. Compared with PD no-ICB, PD-ICB cases showed left precentral and superior frontal cortical thinning, and motor and extramotor white matter tract damage. Compared with controls, all patients had an increased functional connectivity within the visual network. Additionally, PD no-ICB showed increased functional connectivity of bilateral precentral and postcentral gyri within the sensorimotor network compared with controls and PD-ICB. Severity and duration of PD-ICB modulated the functional connectivity between sensorimotor, visual and cognitive networks. Relative to PD no-ICB, PD-ICB patients were characterised by a more severe involvement of frontal, meso-limbic and motor circuits. These data suggest ICB in PD as the result of a disconnection between sensorimotor, associative and cognitive networks with increasing motor impairment, psychiatric symptoms, and ICB duration. These findings may have important implications in understanding the neural substrates underlying ICB in PD.

Self‐reported rates of impulsivity in Parkinson’s Disease

“…Our findings emphasize that impairments to self‐regulation are a key deficiency in the ICB population. While self‐report measures of impulsivity often have only modest to moderate associations with task‐based measures of cognitive functioning and impulsivity, 6,61,77 many PD patients are indeed aware of alterations in cognitive functioning and behavioral changes 78 …”

Intrinsic brain connectivity predicts impulse control disorders in patients with Parkinson's disease

“…The susceptibility of PD patients to impulse control behaviors might be related to a pre‐existing biological predisposition or might occur as a result of dopaminergic medications modulating the neurobiology of PD . Several animal and human studies suggest that these 2 factors may synergistically act on the risk of developing ICD in PD.…”

“…Moreover, patients with PD and ICD seem to present a novelty‐seeking personality, an inclination for risk‐taking behaviors with impaired decision‐making, and motor inhibition . Evidence from previous metabolic, functional, and morphometric imaging studies has consistently demonstrated dysfunction within the meso‐cortico‐limbic‐striatal circuit in patients with PD and ICD, involving both cortical and subcortical areas engaged in the reward system. However, these studies were performed in patients with PD under dopaminergic treatment and with a present history of impulse control behaviors.…”

“…We hypothesized that patients with ICD would show altered intrinsic resting‐state connectivity even before the occurrence of these psychiatric complications. Based on previous studies, we also acquired structural MRIs to explore potential structural changes underlying connectivity abnormalities.…”

MRI of Motor and Nonmotor Therapy‐Induced Complications in Parkinson's Disease

“…Markovic and colleagues showed that PD patients with punding had cortical thinning of the right inferior frontal cortex, reduced functional connectivity between the habenula and frontal cortices, and enhanced functional connectivity of both the habenula and amygdala with the striatum and thalamus, compared with PD patients without ICBs and healthy controls, confirming the crucial role of the frontostriatal circuit in developing ICBs. Imperiale and colleagues showed that PD patients with ICBs had left precentral and superior frontal cortical thinning, together with motor and extramotor white‐matter tract damage. Moreover, the severity and duration of ICBs modulated the functional connectivity between sensorimotor, visual, and cognitive networks.…”