Abstract
Current quantification methods of 123I-FP-CIT SPECT rely on anatomical parcellation of the striatum. We propose here to implement a new method based on MRI segmentation and functional atlas of the basal ganglia (MR-ATLAS) that could provide a reliable quantification within the sensorimotor, associative, and limbic territories of the striatum. Patients with Parkinson’s disease (PD), idiopathic rapid eye movement sleep behavioral disorder (iRBD), and healthy controls underwent 123I-FP-CIT SPECT, MRI, motor, and cognitive assessments. SPECT data were corrected for partial volume effects and registered to a functional atlas of the striatum to allow quantification in every functional region of the striatum (nucleus accumbens, limbic, associative, and sensorimotor parts of the striatum). The MR-ATLAS quantification method is proved to be reliable in every territory of the striatum. In addition, good correlations were found between cognitive dysexecutive tests and the binding within the functional (limbic) territories of the striatum using the MR-ATLAS method, slightly better than correlations found using the anatomical quantification method. This new MR-ATLAS method provides a robust and useful tool for studying the dopaminergic system in PD, particularly with respect to cognitive functions. It may also be relevant to further unravel the relationship between dopaminergic denervation and cognitive or behavioral symptoms.
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Acknowledgements
The authors thank the Clinical Investigations Centre (CIC) for its involvement in the study organization and management, Prof. Richard Levy and Dr. Virginie Czernecki for their helpful discussion around this manuscript, and Dr. Renaud La Joie for his help with the Figures.
ICEBERG study group
Nominated consortia representative: Prof. Marie Vidailhet, MD—Département de Neurologie, Groupe Hospitalier Pitié-Salpêtrière, 47-83 boulevard de l’Hôpital, 75651 PARIS Cedex 13, France, marie.vidailhet@aphp.fr. Steering committee: Marie Vidailhet, MD [(principal investigator of ICEBERG), (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France)], Jean-Christophe Corvol, MD, PhD [(scientific lead), (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France)], Isabelle Arnulf, MD, PhD (member of the steering committee), (Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France; AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Sleep Disorders Unit, Paris, France), Stéphane Lehéricy, MD, PhD (member of the steering committee), (Institut du Cerveau et de la Moelle Epinière—ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France; AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neuroradiology, Paris, France); Clinical data: Marie Vidailhet, MD [(coordination), (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France)], Graziella Mangone, MD, PhD [(co-coordination), (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France)], Jean-Christophe Corvol, MD, PhD (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France), Isabelle Arnulf, MD, PhD (Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France; AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Sleep Disorders Unit, Paris, France), Jonas Ihle, MD (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France), Caroline Weill, MD (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France), David Grabli, MD, PhD (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France), Florence Cormier-Dequaire, MD, PhD (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France), Louise Laure Mariani, MD, PhD (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France), Bertrand Degos, MD, PhD (Service de Neurologie, Hôpital Avicenne, Hôpitaux Universitaires de Paris—Seine Saint Denis, AP-HP, Bobigny, France; Center for Interdisciplinary Research in Biology, Collège de France, INSERM U1050, CNRS UMR7241, Labex Memolife, Paris Sciences et Lettres, Paris, France); Neuropsychological data: Richard Levy, MD, PhD [(coordination), (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France)], Fanny Pineau, MSc [(neuropsychologist), (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France)], Julie Socha, MSc [(neuropsychologist), (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France)], Eve Benchetrit, MSc [(neuropsychologist), (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France)], Virginie Czernecki, PhD [(neuropsychologist), (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France)]; Eye movement: Sophie Rivaud-Pechoux, PhD (coordination), (Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France); Elodie Hainque, MD, PhD (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France); Sleep assessment: Isabelle Arnulf, MD, PhD (coordination), (Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France; AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Sleep Disorders Unit, Paris, France), Smaranda Leu Semenescu, MD (Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France; AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Sleep Disorders Unit, Paris, France), Pauline Dodet, MD (Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France; AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Sleep Disorders Unit, Paris, France); Genetic data: Jean-Christophe Corvol, MD, PhD [(coordination), (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France)], Graziella Mangone, MD, PhD [(co-coordination), (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France)], Samir Bekadar, MSc [(biostatistician), (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France)], Alexis Brice, MD (Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France; AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Genetics, Paris, France), Suzanne Lesage, PhD (genetic analyses) (Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France); Metabolomics: Fanny Mochel, MD, PhD (coordination), (Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France; AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Genetics, Paris, France), Farid Ichou, PhD (ICAN, Pitié-Salpêtrière Hospital, Paris), (Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France; AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Genetics, Paris, France), Vincent Perlbarg, PhD (Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France), Benoit Colsch, PhD (CEA-INRA UMR 0496, DRF/Institut Joliot/SPI, Université Paris-Saclay, MetaboHUB, France), Arthur Tenenhaus, PhD (Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France; L2S Laboratory at CentraleSupélec, France); Brain MRI data: Stéphane Lehericy, MD, PhD (coordination), (Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France; AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neuroradiology, Paris, France), Rahul Gaurav, MS, [(data analysis), (Institut du Cerveau et de la Moelle Epinièrem ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France)], Nadya Pyatigorskaya, MD, PhD (data analysis), (Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France; AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neuroradiology, Paris, France), Lydia Yahia-Cherif, PhD [(Biostatistics), (Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France)], Romain Valabregue, PhD (data analysis) (Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France), Cécile Galléa, PhD (Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France); Datscan imaging data: Marie-Odile Habert, MD (coordination), (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Nuclear Medicine, Paris, France; Sorbonne Université, CNRS, INSERM, Laboratoire d’Imagerie Biomédicale, LIB, Paris, France); Voice recording: Dijana Petrovska, PhD [(Telecom Sud Paris, Evry, coordination), (Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France; TELECOM SudParis, CNRS SAMOVAR UMR 5157, Département Electronique et Physique, MINES TELECOM, Evry, France)], Laetitia Jeancolas, PhD (Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France; TELECOM SudParis, CNRS SAMOVAR UMR 5157, Département Electronique et Physique, MINES TELECOM, Evry, France); Study management: Vanessa Brochard [(coordination), (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France)], Alizé Chalançon [(clinical research assistant), (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France)], Carole Dongmo-Kenfack [(clinical research assistant), (AP-HP Sorbonne Université, Hôpital Pitié-Salpêtrière, Department of Neurology, Paris, France; Institut du Cerveau et de la Moelle Epinière, ICM, Sorbonne Université, INSERM U1127, CNRS 7225, Paris, France)]; study sponsoring: INSERM, Paris.
Funding
IHU-A_ICM ANR‐11‐INBS‐0006, Fondation d'Entreprise EDF, Mr A. Mallart, Energiepole (Belgique), Mr J-J. Legrand and Société Française de Médecine Esthétique (France).
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NV conceived the presented methodological pipeline, contributed to data collection, performed analyses, and wrote the manuscript. GB contributed to data collection and to the writing of the manuscript. M-OH, AK, JCC, GM, SL, MV, and DG contributed to the design of the study, data collection, and writing of manuscript. JA, OJ, RV, and SFV contributed to data analysis.
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Independent of this work, NV received research support from Fondation Bettencourt-Schueller, Fondation Servier and Fondation pour la Recherche sur l’Alzheimer; travel grant from the Movement Disorders Society, Merz-Pharma and GE Healthcare SAS; and is an unpaid sub-investigator in NCT04241068 (aducanumab, Biogen), NCT04437511 (donanemab, Eli-Lilly), NCT04592341 (gantenerumab, Roche), NCT03887455 (lecanemab, Eisai), NCT03352557 (gosuranemab, Biogen), NCT03828747 and NCT03289143 (semorinemab, Roche), NCT04619420 (JNJ-63733657, Janssen—Johnson & Johnson), NCT04374136 (AL001, Alector), NCT04592874 (AL002, Alector). M-OH receives Consultant Fees from the Blue Earth Company. JCC has served in advisory boards for Air Liquide, Biogen, Denali, Ever Pharma, Idorsia, Prevail Therapeutic, Theranexus, UCB; and received grants from Ipsen, the Michael J Fox Foundation, and Sanofi. SL received grants from ‘Investissements d’avenir’ [grant number ANR-10-IAIHU-06 and ANR-11-INBS-0006], Fondation Bettencourt Schuller (Ultrabrain project) and Biogen Inc. DG received grants “Contrat Interface” from INSERM, AP-HP (DRC-PHRC) and France Parkinson, served on scientific advisory boards for AbbVie and Zambon; received research funding from Air Liquide; received speech honorarium from UCB, Teva, Medtronic, Abbvie and Merz; received travel funding from Teva, Novartis, Abbvie and Merz. GB, AK, JA, OJ, RV, SFV, GM, and MV declare no conflict of interest related to this work.
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The study was approved by the local ethic committee Comité de Protection des Personnes (CPP) “Ile-de-France VI” (IRB: 2014-A00725-42/48-14). Informed consent was obtained from all individual participants included in the study.
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Villain, N., Béra, G., Habert, MO. et al. Dopamine denervation in the functional territories of the striatum: a new MR and atlas-based 123I-FP-CIT SPECT quantification method. J Neural Transm 128, 1841–1852 (2021). https://doi.org/10.1007/s00702-021-02434-9
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DOI: https://doi.org/10.1007/s00702-021-02434-9