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Tremor associated with similar structural networks in Parkinson's disease and essential tremor

      Highlights

      • Tremor-dominant PD and ET have high cerebello-thalamo-cortical connectivity.
      • PD is associated with low frontal cortico-subcortical structural connectivity.
      • No correlation between tremor severity and connectivity was found in PD or ET.

      Abstract

      Introduction

      Despite substantial clinical and pathophysiological differences, the characteristics of tremor in Parkinson's disease (PD) and essential tremor (ET) patients bear certain similarities. The presented study delineates tremor-related structural networks in these two disorders.

      Methods

      42 non-advanced PD patients (18 tremor-dominant, 24 without substantial tremor), 17 ET, and 45 healthy controls underwent high-angular resolution diffusion-weighted imaging acquisition to reconstruct their structural motor connectomes as a proxy of the anatomical interconnections between motor network regions, implementing state-of-the-art globally optimised probabilistic tractography.

      Results

      When compared to healthy controls, ET patients exhibited higher structural connectivity in the cerebello-thalamo-cortical network. Interestingly, the comparison of tremor-dominant PD patients and PD patients without tremor yielded very similar results – higher structural connectivity in tremor-dominant PD sharing multiple nodes with the tremor network detected in ET, despite the generally lower structural connectivity between basal ganglia and frontal cortex in the whole PD group when compared to healthy controls.

      Conclusion

      The higher structural connectivity of the cerebello-thalamo-cortical network seems to be the dominant tremor driver in both PD and ET. While it appears to be the only tremor-related network in ET, its combination with large scale hypoconnectivity in the frontal cortico-subcortical network in PD may explain different clinical features of tremor in these two disorders.

      Keywords

      Abbreviations:

      MRI (magnetic resonance imaging), T1w (T1-weighted), T2w (T2-weighted), DWI (diffusion-weighted imaging), HC (healthy controls), PD (Parkinson's disease), PD-TD (tremor-dominant Parkinson's disease), PD-nonTD (Parkinson's disease without tremor), ET (essential tremor)
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      References

        • Uhlhaas P.J.
        • Roux F.
        • Rodriguez E.
        • Rotarska-Jagiela A.
        • Singer W.
        Neural synchrony and the development of cortical networks.
        Trends Cognit. Sci. 2010; 14 (Feb 1): 72-80
        • Hallett M.
        Tremor: pathophysiology.
        Park. Relat. Disord. 2014; 20: S118-S122
        • Bhatia K.P.
        • Bain P.
        • Bajaj N.
        • Elble R.J.
        • Hallett M.
        • Louis E.D.
        • et al.
        Consensus statement on the classification of tremors. From the task force on tremor of the international Parkinson and movement disorder society.
        Mov. Disord. 2018; 33: 75-87
        • Louis E.D.
        • Levy G.
        • Côte L.J.
        • Mejia H.
        • Fahn S.
        • Marder K.
        Clinical correlates of action tremor in Parkinson disease.
        Arch. Neurol. 2001; 58: 1630-1634
        • Fereshtehnejad S.-M.
        • Zeighami Y.
        • Dagher A.
        • Postuma R.B.
        Clinical criteria for subtyping Parkinson's disease: biomarkers and longitudinal progression.
        Brain. 2017; 140: 1959-1976
        • Hallett M.
        Parkinson's disease tremor: pathophysiology.
        Park. Relat. Disord. 2012; 18: S85-S86
        • Piccinin C.C.
        • Campos L.S.
        • Guimarães R.P.
        • Piovesana L.G.
        • Dos Santos M.C.A.
        • Azevedo P.C.
        • et al.
        Differential pattern of cerebellar atrophy in tremor-predominant and akinetic/rigidity-predominant Parkinson's disease.
        Cerebellum. 2017; 16: 623-628
        • Guan X.
        • Xuan M.
        • Gu Q.
        • Xu X.
        • Huang P.
        • Wang N.
        • et al.
        Influence of regional iron on the motor impairments of Parkinson's disease: a quantitative susceptibility mapping study.
        J. Magn. Reson. Imag. 2017; 45: 1335-1342
        • Guan X.
        • Zeng Q.
        • Guo T.
        • Wang J.
        • Xuan M.
        • Gu Q.
        • et al.
        Disrupted functional connectivity of basal ganglia across tremor-dominant and akinetic/rigid-dominant Parkinson's disease.
        Front. Aging Neurosci. 2017; 9: 360
        • Loane C.
        • Wu K.
        • Bain P.
        • Brooks D.J.
        • Piccini P.
        • Politis M.
        Serotonergic loss in motor circuitries correlates with severity of action-postural tremor in PD.
        Neurology. 2013; 80 (May 14): 1850-1855
        • Mure H.
        • Hirano S.
        • Tang C.C.
        • Isaias I.U.
        • Antonini A.
        • Ma Y.
        • et al.
        Parkinson's disease tremor-related metabolic network: characterization, progression, and treatment effects.
        Neuroimage. 2011; 54 (Jan 15): 1244-1253
        • Filip P.
        • Lungu O.V.
        • Manto M.-U.
        • Bareš M.
        Linking essential tremor to the cerebellum: physiological evidence.
        Cerebellum. 2016; 15: 774-780
        • Sporns O.
        • Tononi G.
        • Kötter R.
        The human connectome: a structural description of the human brain.
        PLoS Comput. Biol. 2005; 1: e42
        • Postuma R.B.
        • Berg D.
        • Stern M.
        • Poewe W.
        • Olanow C.W.
        • Oertel W.
        • et al.
        MDS clinical diagnostic criteria for Parkinson's disease.
        Mov. Disord. 2015; 30: 1591-1601
        • Glasser M.F.
        • Sotiropoulos S.N.
        • Wilson J.A.
        • Coalson T.S.
        • Fischl B.
        • Andersson J.L.
        • et al.
        The minimal preprocessing pipelines for the Human Connectome Project.
        Neuroimage. 2013; 80: 105-124
        • Tournier J.-D.
        • Smith R.
        • Raffelt D.
        • Tabbara R.
        • Dhollander T.
        • Pietsch M.
        • et al.
        MRtrix3: a fast, flexible and open software framework for medical image processing and visualisation.
        Neuroimage. 2019; 202: 116137
        • Glasser M.F.
        • Coalson T.S.
        • Robinson E.C.
        • Hacker C.D.
        • Harwell J.
        • Yacoub E.
        • et al.
        A multi-modal parcellation of human cerebral cortex.
        Nature. 2016; 536: 171-178
        • Zalesky A.
        • Fornito A.
        • Bullmore E.T.
        Network-based statistic: identifying differences in brain networks.
        Neuroimage. 2010; 53: 1197-1207
        • Tournier J.-D.
        • Mori S.
        • Leemans A.
        Diffusion tensor imaging and beyond.
        Magn. Reson. Med. 2011; 65: 1532
        • Wichmann T.
        Changing views of the pathophysiology of Parkinsonism.
        Mov. Disord. 2019; 34: 1130-1143
        • Louis E.D.
        • Faust P.L.
        Essential tremor pathology: neurodegeneration and reorganization of neuronal connections.
        Nat. Rev. Neurol. 2020; 16 (Feb): 69-83
        • Cerasa A.
        • Quattrone A.
        Linking essential tremor to the cerebellum—neuroimaging evidence.
        Cerebellum. 2016; 15 (Jun): 263-275
        • Barbagallo G.
        • Caligiuri M.E.
        • Arabia G.
        • Cherubini A.
        • Lupo A.
        • Nisticò R.
        • et al.
        Structural connectivity differences in motor network between tremor-dominant and nontremor Parkinson's disease.
        Hum. Brain Mapp. 2017; 38: 4716-4729
        • Zhang Y.
        • Burock M.A.
        Diffusion tensor imaging in Parkinson's disease and parkinsonian syndrome: a systematic review.
        Front. Neurol. 2020; 11: 1091
        • Seidel K.
        • Bouzrou M.
        • Heidemann N.
        • Krüger R.
        • Schöls L.
        • den Dunnen W.F.
        • et al.
        Involvement of the cerebellum in Parkinson disease and dementia with Lewy bodies.
        Ann. Neurol. 2017; 81: 898-903
        • Cerasa A.
        • Hagberg G.E.
        • Peppe A.
        • Bianciardi M.
        • Gioia M.C.
        • Costa A.
        • et al.
        Functional changes in the activity of cerebellum and frontostriatal regions during externally and internally timed movement in Parkinson's disease.
        Brain Res. Bull. 2006; 71: 259-269
        • Timmermann L.
        • Gross J.
        • Dirks M.
        • Volkmann J.
        • Freund H.
        • Schnitzler A.
        The cerebral oscillatory network of parkinsonian resting tremor.
        Brain. 2003; 126 (Jan 1): 199-212
        • Filip P.
        • Vojtíšek L.
        • Baláž M.
        • Mangia S.
        • Michaeli S.
        • Šumec R.
        • et al.
        Differential diagnosis of tremor syndromes using MRI relaxometry.
        Park. Relat. Disord. 2020; 81: 190-193
        • Parihar R.
        • Alterman R.
        • Papavassiliou E.
        • Tarsy D.
        • Shih L.C.
        Comparison of VIM and STN DBS for Parkinsonian resting and postural/action tremor. Tremor and other hyperkinetic movements.
        . 2015; 5
        • Kok J.G.
        • Leemans A.
        • Teune L.K.
        • Leenders K.L.
        • McKeown M.J.
        • Appel-Cresswell S.
        • et al.
        Structural network analysis using diffusion MRI tractography in Parkinson's disease and correlations with motor impairment.
        Front. Neurol. 2020; 11: 841