학술논문

The neurophysiological brain-fingerprint of Parkinson’s diseaseResearch in context
Document Type
article
Author
Jason da Silva CastanheiraAlex I. WiesmanJustine Y. HansenBratislav MisicSylvain BailletJohn BreitnerJudes PoirierPierre BellecVéronique BohbotMallar ChakravartyLouis CollinsPierre EtienneAlan EvansSerge GauthierRick HogeYasser Ituria-MedinaGerhard MulthaupLisa-Marie MünterNatasha RajahPedro Rosa-NetoJean-Paul SoucyEtienne Vachon-PresseauSylvia VilleneuvePhilippe AmouyelMelissa ApplebyNicholas AshtonDaniel AuldGülebru AyranciChristophe BedettiMarie-Lise BelandKaj BlennowAnn Brinkmalm WestmanClaudio CuelloMahsa DadarLeslie-Ann DaoustSamir DasMarina Dauar-TedeschiLouis De BeaumontDoris DeaMaxime DescoteauxMarianne DufourSarah FarzinFabiola FerdinandVladimir FonovJulie GonneaudJustin KatChristina KazazianAnne LabontéMarie-Elyse Lafaille-MagnanMarc LalancetteJean-Charles LambertJeannie-Marie LeoutsakosLaura MaharAxel MathieuMelissa McSweeneyPierre-François MeyerJustin MironJamie NearHolly NewboldFoxNathalie NilssonPierre OrbanCynthia PicardAlexa Pichet BinetteJean-Baptiste PolineSheida RabipourAlyssa SalaciakMatthew SettimiSivaniya SubramaniapillaiAngela TamChristine TardifLouise ThérouxJennifer Tremblay-MercierStephanie TulloIrem UlkuIsabelle ValléeHenrik ZetterbergVasavan NairJens PruessnerPaul AisenElena AnthalAlan BarkunThomas BeaudryFatiha BenbouhoudJason BrandtLeopoldina CarmoCharles Edouard CarrierLaksanun CheewakriengkraiBlandine CourcotDoris CoutureSuzanne CraftChristian DansereauClément DebackerRené DesautelsSylvie DubucGuerda DuclairMark EisenbergRana El-KhouryAnne-Marie FaubertDavid FontaineJosée FrappierJoanne FrenetteGuylaine GagnéValérie GervaisRenuka GilesRenee GordonClifford JackBenoit JutrasZaven KhachaturianDavid KnopmanPenelope KostopoulosFélix LapalmeTanya LeeClaude LepageIllana LeppertCécile MadjarDavid MailletJean-Robert MaltaisSulantha MathotaarachchiGinette MayrandDiane MichaudThomas MontineJohn MorrisVéronique PagéTharick PascoalSandra PeillieuxMirela PetkovaGalina PogossovaPierre RiouxMark SagerEunice Farah Saint-FortMélissa SavardReisa SperlingShirin TabriziPierre TariotEduard TeignerRonald ThomasPaule-Joanne ToussaintMiranda TuwaigVinod VenugopalanSander VerfaillieJacob VogelKaren WanSeqian WangElsa YuIsabelle Beaulieu-BoirePierre BlanchetSarah BogardManon BouchardSylvain ChouinardFrancesca CicchettiMartin CloutierAlain DagherClotilde DegrootAlex DesautelsMarie Hélène DionJanelle Drouin-OuelletAnne-Marie DufresneNicolas DupréAntoine DuquetteThomas DurcanLesley K. FellowsEdward FonJean-François GagnonZiv Gan-OrAngela GengeNicolas JodoinJason KaramchandaniAnne-Louise LafontaineMélanie LangloisEtienne LeveilleMartin LévesqueCalvin MelmedOury MonchiJacques MontplaisirMichel PanissetMartin ParentMinh-Thy Pham-AnRonald PostumaEmmanuelle PourcherTrisha RaoJean RivestGuy RouleauMadeleine SharpValérie SolandMichael SidelSonia Lai Wing SunAlexander ThielPaolo Vitali
Source
EBioMedicine, Vol 105, Iss , Pp 105201- (2024)
Subject
Movement disorders
Parkinson’s disease
Neural dynamics
Oscillations
Arrhythmic brain activity
Magnetoencephalography
Medicine
Medicine (General)
R5-920
Language
English
ISSN
2352-3964
46662561
Abstract
Summary: Background: Research in healthy young adults shows that characteristic patterns of brain activity define individual “brain-fingerprints” that are unique to each person. However, variability in these brain-fingerprints increases in individuals with neurological conditions, challenging the clinical relevance and potential impact of the approach. Our study shows that brain-fingerprints derived from neurophysiological brain activity are associated with pathophysiological and clinical traits of individual patients with Parkinson’s disease (PD). Methods: We created brain-fingerprints from task-free brain activity recorded through magnetoencephalography in 79 PD patients and compared them with those from two independent samples of age-matched healthy controls (N = 424 total). We decomposed brain activity into arrhythmic and rhythmic components, defining distinct brain-fingerprints for each type from recording durations of up to 4 min and as short as 30 s. Findings: The arrhythmic spectral components of cortical activity in patients with Parkinson’s disease are more variable over short periods, challenging the definition of a reliable brain-fingerprint. However, by isolating the rhythmic components of cortical activity, we derived brain-fingerprints that distinguished between patients and healthy controls with about 90% accuracy. The most prominent cortical features of the resulting Parkinson’s brain-fingerprint are mapped to polyrhythmic activity in unimodal sensorimotor regions. Leveraging these features, we also demonstrate that Parkinson’s symptom laterality can be decoded directly from cortical neurophysiological activity. Furthermore, our study reveals that the cortical topography of the Parkinson’s brain-fingerprint aligns with that of neurotransmitter systems affected by the disease’s pathophysiology. Interpretation: The increased moment-to-moment variability of arrhythmic brain-fingerprints challenges patient differentiation and explains previously published results. We outline patient-specific rhythmic brain signaling features that provide insights into both the neurophysiological signature and symptom laterality of Parkinson’s disease. Thus, the proposed definition of a rhythmic brain-fingerprint of Parkinson’s disease may contribute to novel, refined approaches to patient stratification. Symmetrically, we discuss how rhythmic brain-fingerprints may contribute to the improved identification and testing of therapeutic neurostimulation targets. Funding: Data collection and sharing for this project was provided by the Quebec Parkinson Network (QPN), the Pre-symptomatic Evaluation of Novel or Experimental Treatments for Alzheimer’s Disease (PREVENT-AD; release 6.0) program, the Cambridge Centre for Aging Neuroscience (Cam-CAN), and the Open MEG Archives (OMEGA). The QPN is funded by a grant from Fonds de Recherche du Québec - Santé (FRQS). PREVENT-AD was launched in 2011 as a $13.5 million, 7-year public-private partnership using funds provided by McGill University, the FRQS, an unrestricted research grant from Pfizer Canada, the Levesque Foundation, the Douglas Hospital Research Centre and Foundation, the Government of Canada, and the Canada Fund for Innovation. The Brainstorm project is supported by funding to SB from the NIH (R01-EB026299-05). Further funding to SB for this study included a Discovery grant from the Natural Sciences and Engineering Research Council of Canada of Canada (436355-13), and the CIHR Canada research Chair in Neural Dynamics of Brain Systems (CRC-2017-00311).