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

Molecular Psychiatry volume 23, pages 459–466 (2018)Cite this article

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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.

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Acknowledgements

This study was partially funded by a grant from the Ministry of Education and Science, Republic of Serbia (project 175090).

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Authors and Affiliations

  1. Division of Neuroscience, Neuroimaging Research Unit, Institute of Experimental Neurology, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy

    F Imperiale, F Agosta, E Canu, S Basaia & M Filippi

  2. Clinic of Neurology, Faculty of Medicine, University of Belgrade, Belgrade, Serbia

    V Markovic, M Jecmenica-Lukic, A Tomic & V S Kostic

  3. Unit of Robotics, Brain and Cognitive Sciences, Istituto Italiano di Tecnologia, Genoa, Italy

    A Inuggi

  4. Biostatistics Unit, IRCCS-Ospedale Casa Sollievo della Sofferenza, San Giovanni Rotondo, Foggia, Italy

    M Copetti

  5. Department of Neurology, Division of Neuroscience, Institute of Experimental Neurology, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy

    M Filippi

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Correspondence to M Filippi.

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Competing interests

FA is Section Editor of NeuroImage: Clinical and serves on the editorial board of the Journal of Neurology; has received speaker honoraria from EXCEMED—Excellence in Medical Education; and receives research supports from the Italian Ministry of Health, AriSLA (Fondazione Italiana di Ricerca per la SLA) and the European Research Council. EC has received research support from the Italian Ministry of Health. VM has received research supports from the Ministry of Education and Science, Republic of Serbia. AI has received research supports from AriSLA—Fondazione Italiana di Ricerca per la Sclerosi Laterale Amiotrofica. MC has received compensation for consulting and/or serving on advisory boards from Teva Pharmaceuticals and Biogen Idec. VSK serves on the editorial board of the Journal of Neurology; and has received research grants from Ministry of Education and Science, Republic of Serbia and the Serbian Academy of Science and Arts; he receives research supports from Valeant, Stada, Novartis and Boehriner Ingelheim, and speaker honoraria from Novartis and Boehringer Ingelheim. MF is Editor-in-Chief of the Journal of Neurology; serves on a scientific advisory board for Teva Pharmaceutical Industries; has received compensation for consulting services and/or speaking activities from Biogen Idec, ExceMED, Novartis and Teva Pharmaceutical Industries; and receives research support from Biogen Idec, Teva Pharmaceutical Industries, Novartis, Italian Ministry of Health, Fondazione Italiana Sclerosi Multipla, Cure PSP, Alzheimer's Drug Discovery Foundation (ADDF), the Jacques and Gloria Gossweiler Foundation (Switzerland) and ARiSLA (Fondazione Italiana di Ricerca per la SLA). The remaining authors declare no conflict of interest.

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Imperiale, F., Agosta, F., Canu, E. et al. Brain structural and functional signatures of impulsive–compulsive behaviours in Parkinson’s disease. Mol Psychiatry 23, 459–466 (2018). https://doi.org/10.1038/mp.2017.18

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