Parkinsonian central pain is linked to the connectivity of the nucleus accumbens and the anterior insula

Pain is a frequent and disabling non-motor symptom of Parkinson’s Disease (PD). Yet, no treatment to date can efficiently reduce this pain. This article investigates the brain functional connectivity of PD patients with central pain and the effects of levodopa and oxycodone on this connectivity.Thir...

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Main Authors: Karel Joineau, Mathilde Boussac, Patrice Peran, David Devos, Jean Luc Houeto, Sophie Drapier, David Maltete, Jesus Aguilar, Estelle Harroch, Margherita Fabbri, Clémence Leung, Fabienne Ory-Magne, Melissa Tir, Christine Tranchant, Hayet Salhi, Solène Frismand, Frederique Fluchere, Ana Marques, Olivier Rascol, Emeline Descamps, Christine Brefel-Courbon
Format: Article
Language:English
Published: Elsevier 2024-03-01
Series:NeuroImage: Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2666956024000035
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author Karel Joineau
Mathilde Boussac
Patrice Peran
David Devos
Jean Luc Houeto
Sophie Drapier
David Maltete
Jesus Aguilar
Estelle Harroch
Margherita Fabbri
Clémence Leung
Fabienne Ory-Magne
Melissa Tir
Christine Tranchant
Hayet Salhi
Solène Frismand
Frederique Fluchere
Ana Marques
Olivier Rascol
Emeline Descamps
Christine Brefel-Courbon
author_facet Karel Joineau
Mathilde Boussac
Patrice Peran
David Devos
Jean Luc Houeto
Sophie Drapier
David Maltete
Jesus Aguilar
Estelle Harroch
Margherita Fabbri
Clémence Leung
Fabienne Ory-Magne
Melissa Tir
Christine Tranchant
Hayet Salhi
Solène Frismand
Frederique Fluchere
Ana Marques
Olivier Rascol
Emeline Descamps
Christine Brefel-Courbon
author_sort Karel Joineau
collection DOAJ
description Pain is a frequent and disabling non-motor symptom of Parkinson’s Disease (PD). Yet, no treatment to date can efficiently reduce this pain. This article investigates the brain functional connectivity of PD patients with central pain and the effects of levodopa and oxycodone on this connectivity.Thirty-eight PD patients received either levodopa, oxycodone, or a placebo during an eight-week period. Pain intensity was evaluated using the Visual Analogue Scale and resting-state functional connectivity was measured before and after treatments. PD patients were also separated into two groups: responders and non-responders.At baseline, the intensity of pain was correlated with the connectivity between the anterior insula and the posterior cingulate cortex and between the nucleus accumbens, the brainstem, and the hippocampus. Levodopa and oxycodone had no specific effects on functional connectivity. Responders had a decrease in connectivity between the anterior insula and the posterior cingulate cortex, while non-responders showed an increase in connectivity.The correlation between pain intensity and specific brain connectivity may represent a “hyper-awareness” of pain and a distortion of learning and memory systems in PD patients with central pain, leading to a state of chronic pain. The placebo effect could explain the changes in connectivity that are associated with a potential reduction in pain awareness.
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spelling doaj-art-5a0fbaea3c094a329e4238ff626c33892025-08-20T03:34:31ZengElsevierNeuroImage: Reports2666-95602024-03-014110019710.1016/j.ynirp.2024.100197Parkinsonian central pain is linked to the connectivity of the nucleus accumbens and the anterior insulaKarel Joineau0Mathilde Boussac1Patrice Peran2David Devos3Jean Luc Houeto4Sophie Drapier5David Maltete6Jesus Aguilar7Estelle Harroch8Margherita Fabbri9Clémence Leung10Fabienne Ory-Magne11Melissa Tir12Christine Tranchant13Hayet Salhi14Solène Frismand15Frederique Fluchere16Ana Marques17Olivier Rascol18Emeline Descamps19Christine Brefel-Courbon20Toulouse NeuroImaging Centre (ToNIC – UMR1214 INSERM/UT3), Toulouse, France; Corresponding author.Toulouse NeuroImaging Centre (ToNIC – UMR1214 INSERM/UT3), Toulouse, FranceToulouse NeuroImaging Centre (ToNIC – UMR1214 INSERM/UT3), Toulouse, FranceDepartment of Medical Pharmacology, Department of Neurology, Expert Center of Parkinson’s Disease, Université de Lille, Lille, Lille Neuroscience and Cognition INSERM 1172, CHU de Lille NS-PARK Network, FranceParkinson Expert Center, Neurology Department, Limoges University Hospital, U1094 Inserm UMR270 IRD USC1501 INRAE Epidémiologie des Maladies Chroniques en Zone Tropicale EpiMaCT, Limoges, France; Clinical Investigation Center INSERM 1402, Poitiers University Hospital, Poitiers, FranceDepartment of Neurology, Pontchaillou Rennes University Hospital, Clinical Investigation Center Inserm 1414, Rennes, FranceDepartment of Neurology, Rouen University Hospital and University of Rouen, France; INSERM U1239, Laboratory of Neuronal and Neuroendocrine Differentiation and Communication, Mont-Saint-Aignan, France; NS-Park French Network, FranceDepartment of Neuroradiology, Nantes University Hospital, Nantes, FranceDepartment of Clinical Pharmacology and Neurology, University Hospital of Toulouse, Toulouse, FranceToulouse NeuroImaging Centre (ToNIC – UMR1214 INSERM/UT3), Toulouse, France; Department of Clinical Pharmacology and Neurology, University Hospital of Toulouse, Toulouse, FranceDepartment of Clinical Pharmacology and Neurology, University Hospital of Toulouse, Toulouse, FranceToulouse NeuroImaging Centre (ToNIC – UMR1214 INSERM/UT3), Toulouse, France; Department of Clinical Pharmacology and Neurology, University Hospital of Toulouse, Toulouse, FranceDepartment of Neurology, Parkinson Expert Center, Amiens University Hospital, Amiens, FranceNeurology Department, Strasbourg University Hospital, Strasbourg, France; Strasbourg Federation of Translational Medicine, Strasbourg University, Strasbourg, France; Institute of Genetics and Cellular and Molecular Biology, INSERM-U964, CNRS-UMR7104, University of Strasbourg, Illkirch-Graffenstaden, FranceDepartment of Neurology, Parkinson Expert Center, Henri Mondor University Hospital, Assistance Publique - Hôpitaux de Paris, Créteil, FranceDepartment of Neurology, Nancy University Hospital, Nancy, FranceDepartment of Neurology and Movement Disorders, Timone University Hospital, Assistance Publique - Hôpitaux de Marseille, FranceDepartment of Neurology, CHU Clermont-Ferrand, Université Clermont-Auvergne, CNRS, ICCN, Institut Pascal, Clermont-Ferrand, NS-Park/F-CRIN Network, FranceClinical Investigation Center CIC1436, Departments of Clinical Pharmacology and Neurosciences, NS-Park/FCRIN Network and NeuroToul COEN Center, University of Toulouse, INSERM and University of Toulouse 3, Toulouse, FranceToulouse NeuroImaging Centre (ToNIC – UMR1214 INSERM/UT3), Toulouse, France; CNRS Toulouse, FranceToulouse NeuroImaging Centre (ToNIC – UMR1214 INSERM/UT3), Toulouse, France; Department of Clinical Pharmacology and Neurology, University Hospital of Toulouse, Toulouse, FrancePain is a frequent and disabling non-motor symptom of Parkinson’s Disease (PD). Yet, no treatment to date can efficiently reduce this pain. This article investigates the brain functional connectivity of PD patients with central pain and the effects of levodopa and oxycodone on this connectivity.Thirty-eight PD patients received either levodopa, oxycodone, or a placebo during an eight-week period. Pain intensity was evaluated using the Visual Analogue Scale and resting-state functional connectivity was measured before and after treatments. PD patients were also separated into two groups: responders and non-responders.At baseline, the intensity of pain was correlated with the connectivity between the anterior insula and the posterior cingulate cortex and between the nucleus accumbens, the brainstem, and the hippocampus. Levodopa and oxycodone had no specific effects on functional connectivity. Responders had a decrease in connectivity between the anterior insula and the posterior cingulate cortex, while non-responders showed an increase in connectivity.The correlation between pain intensity and specific brain connectivity may represent a “hyper-awareness” of pain and a distortion of learning and memory systems in PD patients with central pain, leading to a state of chronic pain. The placebo effect could explain the changes in connectivity that are associated with a potential reduction in pain awareness.http://www.sciencedirect.com/science/article/pii/S2666956024000035Parkinson’s diseasePainResting stateFunctional connectivityLevodopaOxycodone
spellingShingle Karel Joineau
Mathilde Boussac
Patrice Peran
David Devos
Jean Luc Houeto
Sophie Drapier
David Maltete
Jesus Aguilar
Estelle Harroch
Margherita Fabbri
Clémence Leung
Fabienne Ory-Magne
Melissa Tir
Christine Tranchant
Hayet Salhi
Solène Frismand
Frederique Fluchere
Ana Marques
Olivier Rascol
Emeline Descamps
Christine Brefel-Courbon
Parkinsonian central pain is linked to the connectivity of the nucleus accumbens and the anterior insula
NeuroImage: Reports
Parkinson’s disease
Pain
Resting state
Functional connectivity
Levodopa
Oxycodone
title Parkinsonian central pain is linked to the connectivity of the nucleus accumbens and the anterior insula
title_full Parkinsonian central pain is linked to the connectivity of the nucleus accumbens and the anterior insula
title_fullStr Parkinsonian central pain is linked to the connectivity of the nucleus accumbens and the anterior insula
title_full_unstemmed Parkinsonian central pain is linked to the connectivity of the nucleus accumbens and the anterior insula
title_short Parkinsonian central pain is linked to the connectivity of the nucleus accumbens and the anterior insula
title_sort parkinsonian central pain is linked to the connectivity of the nucleus accumbens and the anterior insula
topic Parkinson’s disease
Pain
Resting state
Functional connectivity
Levodopa
Oxycodone
url http://www.sciencedirect.com/science/article/pii/S2666956024000035
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