The Role of Cerebellum and Basal Ganglia Functional Connectivity in Altered Voluntary Movement Execution in Essential Tremor.

Dentate nucleus Essential tremor Globus pallidus Kinematic analysis Resting state functional connectivity

Journal

Cerebellum (London, England)
ISSN: 1473-4230
Titre abrégé: Cerebellum
Pays: United States
ID NLM: 101089443

Informations de publication

Date de publication:
18 May 2024
Historique:
accepted: 25 04 2024
medline: 18 5 2024
pubmed: 18 5 2024
entrez: 18 5 2024
Statut: aheadofprint

Résumé

Substantial evidence highlights the role of the cerebellum in the pathophysiology of tremor in essential tremor (ET), although its potential involvement in altered movement execution in this condition remains unclear. This study aims to explore potential correlations between the cerebellum and basal ganglia functional connectivity and voluntary movement execution abnormalities in ET, objectively assessed with kinematic techniques. A total of 20 patients diagnosed with ET and 18 healthy subjects were enrolled in this study. Tremor and repetitive finger tapping were recorded using an optoelectronic kinematic system. All participants underwent comprehensive 3T-MRI examinations, including 3D-T1 and blood-oxygen-level dependent (BOLD) sequences during resting state. Morphometric analysis was conducted on the 3D-T1 images, while a seed-based analysis was performed to investigate the resting-state functional connectivity (rsFC) of dorsal and ventral portions of the dentate nucleus and the external and internal segments of the globus pallidus. Finally, potential correlations between rsFC alterations in patients and clinical as well as kinematic scores were assessed. Finger tapping movements were slower in ET than in healthy subjects. Compared to healthy subjects, patients with ET exhibited altered FC of both dentate and globus pallidus with cerebellar, basal ganglia, and cortical areas. Interestingly, both dentate and pallidal FC exhibited positive correlations with movement velocity in patients, differently from that we observed in healthy subjects, indicating the higher the FC, the faster the finger tapping. The findings of this study indicate the possible role of both cerebellum and basal ganglia in the pathophysiology of altered voluntary movement execution in patients with ET.

Identifiants

pubmed: 38761352
doi: 10.1007/s12311-024-01699-6
pii: 10.1007/s12311-024-01699-6
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s).

Références

Bhatia KP, Bain P, Bajaj N, Elble RJ, Hallett M, Louis ED, Raethjen J, Stamelou M, Testa CM, Deuschl G, the Tremor Task Force of the International Parkinson and Movement Disorder Society. Consensus Statement on the classification of tremors. from the task force on tremor of the International Parkinson and Movement Disorder Society: IPMDS Task Force on Tremor Consensus Statement. Mov Disord. 2018;33:75–87. https://doi.org/10.1002/mds.27121 .
doi: 10.1002/mds.27121 pubmed: 29193359
Bologna M, Paparella G, Colella D, Cannavacciuolo A, Angelini L, Alunni-Fegatelli D, Guerra A, Berardelli A. Is there evidence of bradykinesia in essential tremor? Eur J Neurol. 2020;27:1501–9. https://doi.org/10.1111/ene.14312 .
doi: 10.1111/ene.14312 pubmed: 32396976
Duval C, Sadikot AF, Panisset M. Bradykinesia in patients with essential tremor. Brain Res. 2006;1115:213–6. https://doi.org/10.1016/j.brainres.2006.07.066 .
doi: 10.1016/j.brainres.2006.07.066 pubmed: 16920079
Goubault E, Nguyen HP, Ayachi FS, Bogard S, Duval C. Do Bradykinesia and Tremor Interfere in Voluntary Movement of Essential Tremor Patients? Preliminary Findings. Tremor Hyperkinetic Mov. 2017;7:459. https://doi.org/10.5334/tohm.341 .
doi: 10.5334/tohm.341
Jiménez-Jiménez FJ, Rubio L, Alonso-Navarro H, Calleja M, Pilo-de-la-Fuente B, Plaza-Nieto JF, Benito-León J, García-Ruiz PJ, Agúndez JAG. Impairment of rapid repetitive finger movements and visual reaction time in patients with essential tremor: Motor performance in essential tremor. Eur J Neurol. 2010;17:152–9. https://doi.org/10.1111/j.1468-1331.2009.02784.x .
doi: 10.1111/j.1468-1331.2009.02784.x pubmed: 19765055
Bologna M, Espay AJ, Fasano A, Paparella G, Hallett M, Berardelli A. Redefining Bradykinesia. Mov Disord Off J Mov Disord Soc. 2023;38:551–7. https://doi.org/10.1002/mds.29362 .
doi: 10.1002/mds.29362
Paparella G, Fasano A, Hallett M, Berardelli A, Bologna M. Emerging concepts on bradykinesia in non-parkinsonian conditions. Eur J Neurol. 2021. https://doi.org/10.1111/ene.14851 .
doi: 10.1111/ene.14851 pubmed: 33793037
Benito-León J, Labiano-Fontcuberta A. Linking Essential Tremor to the Cerebellum: Clinical Evidence. The Cerebellum. 2016;15:253–62. https://doi.org/10.1007/s12311-015-0741-1 .
doi: 10.1007/s12311-015-0741-1 pubmed: 26521074
Fanning A, Kuo S-H. Clinical Heterogeneity of Essential Tremor: Understanding Neural Substrates of Action Tremor Subtypes. The Cerebellum. 2023. https://doi.org/10.1007/s12311-023-01551-3 .
doi: 10.1007/s12311-023-01551-3 pubmed: 37022657
Haubenberger D, Hallett M. Essential Tremor. N Engl J Med. 2018;378:1802–10. https://doi.org/10.1056/NEJMcp1707928 .
doi: 10.1056/NEJMcp1707928 pubmed: 29742376
Helmich RC, Toni I, Deuschl G, Bloem BR. The Pathophysiology of Essential Tremor and Parkinson’s Tremor. Curr Neurol Neurosci Rep. 2013;13:378. https://doi.org/10.1007/s11910-013-0378-8 .
doi: 10.1007/s11910-013-0378-8 pubmed: 23893097
Muthuraman M, Heute U, Arning K, Anwar AR, Elble R, Deuschl G, Raethjen J. Oscillating central motor networks in pathological tremors and voluntary movements What makes the difference? NeuroImage. 2012;60:1331–9. https://doi.org/10.1016/j.neuroimage.2012.01.088 .
doi: 10.1016/j.neuroimage.2012.01.088 pubmed: 22293134
Bédard P, Panyakaew P, Cho H-J, Hallett M, Horovitz SG. Multimodal imaging of essential tremor and dystonic tremor. NeuroImage Clin. 2022;36:103247. https://doi.org/10.1016/j.nicl.2022.103247 .
doi: 10.1016/j.nicl.2022.103247 pubmed: 36451353 pmcid: 9668651
Mueller K, Jech R, Hoskovcová M, Ulmanová O, Urgošík D, Vymazal J, Růžička E. General and selective brain connectivity alterations in essential tremor: A resting state fMRI study. NeuroImage Clin. 2017;16:468–76. https://doi.org/10.1016/j.nicl.2017.06.004 .
doi: 10.1016/j.nicl.2017.06.004 pubmed: 28913163 pmcid: 5587870
Nicoletti V, Cecchi P, Pesaresi I, Frosini D, Cosottini M, Ceravolo R. Cerebello-thalamo-cortical network is intrinsically altered in essential tremor: evidence from a resting state functional MRI study. Sci Rep. 2020;10:16661. https://doi.org/10.1038/s41598-020-73714-9 .
doi: 10.1038/s41598-020-73714-9 pubmed: 33028912 pmcid: 7541442
Pietracupa S, Bologna M, Tommasin S, Berardelli A, Pantano P. The Contribution of Neuroimaging to the Understanding of Essential Tremor Pathophysiology: a Systematic Review. The Cerebellum. 2021;21:1029–51. https://doi.org/10.1007/s12311-021-01335-7 .
doi: 10.1007/s12311-021-01335-7 pubmed: 34657271
Tikoo S, Pietracupa S, Tommasin S, Bologna M, Petsas N, Bharti K, Berardelli A, Pantano P. Functional disconnection of the dentate nucleus in essential tremor. J Neurol. 2020;267:1358–67. https://doi.org/10.1007/s00415-020-09711-9 .
doi: 10.1007/s00415-020-09711-9 pubmed: 31974808
Matano S. Brief communication: Proportions of the ventral half of the cerebellar dentate nucleus in humans and great apes. Am J Phys Anthropol. 2001;114:163–5. https://doi.org/10.1002/1096-8644(200102)114:2%3c163::AID-AJPA1016%3e3.0.CO;2-F .
doi: 10.1002/1096-8644(200102)114:2<163::AID-AJPA1016>3.0.CO;2-F pubmed: 11169906
Hoover JE, Strick PL. The organization of cerebellar and basal ganglia outputs to primary motor cortex as revealed by retrograde transneuronal transport of herpes simplex virus type 1. J Neurosci Off J Soc Neurosci. 1999;19:1446–63. https://doi.org/10.1523/JNEUROSCI.19-04-01446.1999 .
doi: 10.1523/JNEUROSCI.19-04-01446.1999
Middleton FA, Strick PL. Cerebellar output channels. Int Rev Neurobiol. 1997;41:61–82. https://doi.org/10.1016/s0074-7742(08)60347-5 .
doi: 10.1016/s0074-7742(08)60347-5 pubmed: 9378611
Middleton FA, Strick PL. Cerebellar projections to the prefrontal cortex of the primate. J Neurosci Off J Soc Neurosci. 2001;21:700–12. https://doi.org/10.1523/JNEUROSCI.21-02-00700.2001 .
doi: 10.1523/JNEUROSCI.21-02-00700.2001
Hoshi E, Tremblay L, Féger J, Carras PL, Strick PL. The cerebellum communicates with the basal ganglia. Nat Neurosci. 2005;8:1491–3. https://doi.org/10.1038/nn1544 .
doi: 10.1038/nn1544 pubmed: 16205719
Buijink AWG, Broersma M, van der Stouwe AMM, van Wingen GA, Groot PFC, Speelman JD, Maurits NM, van Rootselaar AF. Rhythmic finger tapping reveals cerebellar dysfunction in essential tremor. Parkinsonism Relat Disord. 2015;21:383–8. https://doi.org/10.1016/j.parkreldis.2015.02.003 .
doi: 10.1016/j.parkreldis.2015.02.003 pubmed: 25703340
Wu T, Hallett M. The cerebellum in Parkinson’s disease. Brain. 2013;136:696–709. https://doi.org/10.1093/brain/aws360 .
doi: 10.1093/brain/aws360 pubmed: 23404337 pmcid: 7273201
Bologna M, Paparella G, Fasano A, Hallett M, Berardelli A. Evolving concepts on bradykinesia. Brain J Neurol. 2020;143:727–50. https://doi.org/10.1093/brain/awz344 .
doi: 10.1093/brain/awz344
Redgrave P, Rodriguez M, Smith Y, Rodriguez-Oroz MC, Lehericy S, Bergman H, Agid Y, DeLong MR, Obeso JA. Goal-directed and habitual control in the basal ganglia: implications for Parkinson’s disease. Nat Rev Neurosci. 2010;11:760–72. https://doi.org/10.1038/nrn2915 .
doi: 10.1038/nrn2915 pubmed: 20944662 pmcid: 3124757
Jahanshahi M, Obeso I, Rothwell JC, Obeso JA. A fronto–striato–subthalamic–pallidal network for goal-directed and habitual inhibition. Nat Rev Neurosci. 2015;16:719–32. https://doi.org/10.1038/nrn4038 .
doi: 10.1038/nrn4038 pubmed: 26530468
Jaeger D, Kita H. Functional connectivity and integrative properties of globus pallidus neurons. Neuroscience. 2011;198:44–53. https://doi.org/10.1016/j.neuroscience.2011.07.050 .
doi: 10.1016/j.neuroscience.2011.07.050 pubmed: 21835227
Blenkinsop A, Anderson S, Gurney K. Frequency and function in the basal ganglia: the origins of beta and gamma band activity. J Physiol. 2017;595:4525–48. https://doi.org/10.1113/JP273760 .
doi: 10.1113/JP273760 pubmed: 28334424 pmcid: 5491879
Nishibayashi H, Ogura M, Kakishita K, Tanaka S, Tachibana Y, Nambu A, Kita H, Itakura T. Cortically evoked responses of human pallidal neurons recorded during stereotactic neurosurgery. Mov Disord. 2011;26:469–76. https://doi.org/10.1002/mds.23502 .
doi: 10.1002/mds.23502 pubmed: 21312279
Villalobos N, Almazán-Alvarado S, Magdaleno-Madrigal VM. Elevation of GABA levels in the globus pallidus disinhibits the thalamic reticular nucleus and desynchronized cortical beta oscillations. J Physiol Sci JPS. 2022;72:17. https://doi.org/10.1186/s12576-022-00843-3 .
doi: 10.1186/s12576-022-00843-3 pubmed: 35896962
Caligiuri ME, Arabia G, Barbagallo G, Lupo A, Morelli M, Nisticò R, Novellino F, Quattrone A, Salsone M, Vescio B, Cherubini A, Quattrone A. Structural connectivity differences in essential tremor with and without resting tremor. J Neurol. 2017;264:1865–74. https://doi.org/10.1007/s00415-017-8553-5 .
doi: 10.1007/s00415-017-8553-5 pubmed: 28730570
Colella D, Passaretti M, Frantellizzi V, Silvia De Feo M, Cannavacciuolo A, Angelini L, Birreci D, Costa D, Paparella G, Guerra A, De Vincentis G, Berardelli A, Bologna M. Subtle changes in central dopaminergic tone underlie bradykinesia in essential tremor. NeuroImage Clin. 2023;40:103526. https://doi.org/10.1016/j.nicl.2023.103526 .
doi: 10.1016/j.nicl.2023.103526 pubmed: 37847966 pmcid: 10587600
Bologna M, Leodori G, Stirpe P, Paparella G, Colella D, Belvisi D, Fasano A, Fabbrini G, Berardelli A. Bradykinesia in early and advanced Parkinson’s disease. J Neurol Sci. 2016;369:286–91. https://doi.org/10.1016/j.jns.2016.08.028 .
doi: 10.1016/j.jns.2016.08.028 pubmed: 27653910
Elble R, Comella C, Fahn S, Hallett M, Jankovic J, Juncos JL, LeWitt P, Lyons K, Ondo W, Pahwa R, Sethi K, Stover N, Tarsy D, Testa C, Tintner R, Watts R, Zesiewicz T. Reliability of a new scale for essential tremor. Mov Disord. 2012;27:1567–9. https://doi.org/10.1002/mds.25162 .
doi: 10.1002/mds.25162 pubmed: 23032792 pmcid: 4157921
MDS-UPDRS Italian Validation Study Group, Antonini A, Abbruzzese G, Ferini-Strambi L, Tilley B, Huang J, Stebbins GT, Goetz CG, Barone P, Bandettini di Poggio M, Fabbrini G, Di Stasio F, Tinazzi M, Bovi T, Ramat S, Meoni S, Pezzoli G, Canesi M, Martinelli P, Maria Scaglione CL, Rossi A, Tambasco N, Santangelo G, Picillo M, Morgante L, Morgante F, Quatrale R, Sensi M, Pilleri M, Biundo R, Nordera G, Caria A, Pacchetti C, Zangaglia R, Lopiano L, Zibetti M, Zappia M, Nicoletti A, Quattrone A, Salsone M, Cossu G, Murgia D, Albanese A, Del Sorbo F. Validation of the Italian version of the Movement Disorder Society—Unified Parkinson’s Disease Rating Scale. Neurol Sci. 2013. 34:683–687 https://doi.org/10.1007/s10072-012-1112-z
Freitas S, Simões MR, Alves L, Santana I. Montreal Cognitive Assessment: Validation Study for Mild Cognitive Impairment and Alzheimer Disease. Alzheimer Dis Assoc Disord. 2013;27:37–43. https://doi.org/10.1097/WAD.0b013e3182420bfe .
doi: 10.1097/WAD.0b013e3182420bfe pubmed: 22193353
Beck AT. An Inventory for Measuring Depression. Arch Gen Psychiatry. 1961;4:561. https://doi.org/10.1001/archpsyc.1961.01710120031004 .
doi: 10.1001/archpsyc.1961.01710120031004 pubmed: 13688369
Colella D, Guerra A, Paparella G, Cioffi E, Di Vita A, Trebbastoni A, Berardelli A, Bologna M. Motor dysfunction in mild cognitive impairment as tested by kinematic analysis and transcranial magnetic stimulation. Clin Neurophysiol. 2021;132:315–22. https://doi.org/10.1016/j.clinph.2020.10.028 .
doi: 10.1016/j.clinph.2020.10.028 pubmed: 33450553
Paparella G, Angelini L, De Biase A, Cannavacciuolo A, Colella D, Di Bonaventura C, Giallonardo AT, Berardelli A, Bologna M. Clinical and Kinematic Features of Valproate-Induced Tremor and Differences with Essential Tremor. Cerebellum Lond Engl. 2020. https://doi.org/10.1007/s12311-020-01216-5 .
doi: 10.1007/s12311-020-01216-5
Paparella G, Ferrazzano G, Cannavacciuolo A, Cogliati Dezza F, Fabbrini G, Bologna M, Berardelli A. Differential effects of propranolol on head and upper limb tremor in patients with essential tremor and dystonia. J Neurol. 2018. https://doi.org/10.1007/s00415-018-9052-z .
Angelini L, Paparella G, De Biase A, Maraone A, Panfili M, Berardelli I, Cannavacciuolo A, Di Vita A, Margiotta R, Fabbrini G, Berardelli A, Bologna M. Longitudinal study of clinical and neurophysiological features in essential tremor. Eur J Neurol. 2022. https://doi.org/10.1111/ene.15650 .
doi: 10.1111/ene.15650 pubmed: 36437695 pmcid: 10107502
Passaretti M, De Biase A, Paparella G, Angelini L, Cannavacciuolo A, Colella D, Berardelli A, Bologna M. Worsening of Essential Tremor After SARS-CoV-2 Infection. Cerebellum Lond Engl. 2022. https://doi.org/10.1007/s12311-022-01366-8 .
doi: 10.1007/s12311-022-01366-8
Smith SM, Zhang Y, Jenkinson M, Chen J, Matthews PM, Federico A, De Stefano N. Accurate, Robust, and Automated Longitudinal and Cross-Sectional Brain Change Analysis. NeuroImage. 2002;17:479–89. https://doi.org/10.1006/nimg.2002.1040 .
doi: 10.1006/nimg.2002.1040 pubmed: 12482100
Pruim RHR, Mennes M, Buitelaar JK, Beckmann CF. Evaluation of ICA-AROMA and alternative strategies for motion artifact removal in resting state fMRI. NeuroImage. 2015;112:278–87. https://doi.org/10.1016/j.neuroimage.2015.02.063 .
doi: 10.1016/j.neuroimage.2015.02.063 pubmed: 25770990
Anteraper SA, Guell X, Taylor HP, D’Mello A, Whitfield-Gabrieli S, Joshi G. Intrinsic Functional Connectivity of Dentate Nuclei in Autism Spectrum Disorder. Brain Connect. 2019;9:692–702. https://doi.org/10.1089/brain.2019.0692 .
doi: 10.1089/brain.2019.0692 pubmed: 31591901 pmcid: 7058992
Bernard JA, Peltier SJ, Benson BL, Wiggins JL, Jaeggi SM, Buschkuehl M, Jonides J, Monk CS, Seidler RD. Dissociable functional networks of the human dentate nucleus. Cereb Cortex N Y N. 2014;1991(24):2151–9. https://doi.org/10.1093/cercor/bht065 .
doi: 10.1093/cercor/bht065
Tarcijonas G, Foran W, Haas GL, Luna B, Sarpal DK. Intrinsic Connectivity of the Globus Pallidus: An Uncharted Marker of Functional Prognosis in People With First-Episode Schizophrenia. Schizophr Bull. 2020;46:184–92. https://doi.org/10.1093/schbul/sbz034 .
doi: 10.1093/schbul/sbz034 pubmed: 31150557
Benjamini Y, Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J R Stat Soc Ser B Methodol. 1995;57:289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x .
doi: 10.1111/j.2517-6161.1995.tb02031.x
Postuma RB, Berg D, Stern M, Poewe W, Olanow CW, Oertel W, Obeso J, Marek K, Litvan I, Lang AE, Halliday G, Goetz CG, Gasser T, Dubois B, Chan P, Bloem BR, Adler CH, Deuschl G. MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord Off J Mov Disord Soc. 2015;30:1591–601. https://doi.org/10.1002/mds.26424 .
doi: 10.1002/mds.26424
Holtbernd F, Shah NJ. Imaging the Pathophysiology of Essential Tremor-A Systematic Review. Front Neurol. 2021;12:680254. https://doi.org/10.3389/fneur.2021.680254 .
doi: 10.3389/fneur.2021.680254 pubmed: 34220687 pmcid: 8244929
Luo R, Pan P, Xu Y, Chen L. No reliable gray matter changes in essential tremor. Neurol Sci Off J Ital Neurol Soc Ital Soc Clin Neurophysiol. 2019;40:2051–63. https://doi.org/10.1007/s10072-019-03933-0 .
doi: 10.1007/s10072-019-03933-0
Pietracupa S, Bologna M, Bharti K, Pasqua G, Tommasin S, Elifani F, Paparella G, Petsas N, Grillea G, Berardelli A, Pantano P. White matter rather than gray matter damage characterizes essential tremor. Eur Radiol. 2019;29:6634–42. https://doi.org/10.1007/s00330-019-06267-9 .
doi: 10.1007/s00330-019-06267-9 pubmed: 31139970
Novellino F, Cherubini A, Chiriaco C, Morelli M, Salsone M, Arabia G, Quattrone A. Brain iron deposition in essential tremor: a quantitative 3-Tesla magnetic resonance imaging study. Mov Disord Off J Mov Disord Soc. 2013;28:196–200. https://doi.org/10.1002/mds.25263 .
doi: 10.1002/mds.25263
Fang W, Chen H, Wang H, Zhang H, Puneet M, Liu M, Lv F, Luo T, Cheng O, Wang X, Lu X. Essential tremor is associated with disruption of functional connectivity in the ventral intermediate Nucleus-Motor Cortex–Cerebellum circuit. Hum Brain Mapp. 2016;37:165–78. https://doi.org/10.1002/hbm.23024 .
doi: 10.1002/hbm.23024 pubmed: 26467643
Buijink AWG, van der Stouwe AMM, Broersma M, Sharifi S, Groot PFC, Speelman JD, Maurits NM, van Rootselaar A-F. Motor network disruption in essential tremor: a functional and effective connectivity study. Brain. 2015;138:2934–47. https://doi.org/10.1093/brain/awv225 .
doi: 10.1093/brain/awv225 pubmed: 26248468
Lenka A, Bhalsing KS, Panda R, Jhunjhunwala K, Naduthota RM, Saini J, Bharath RD, Yadav R, Pal PK. Role of altered cerebello-thalamo-cortical network in the neurobiology of essential tremor. Neuroradiology. 2017;59:157–68. https://doi.org/10.1007/s00234-016-1771-1 .
doi: 10.1007/s00234-016-1771-1 pubmed: 28062908
Benito-León J, Sanz-Morales E, Melero H, Louis ED, Romero JP, Rocon E, Malpica N. Graph theory analysis of resting-state functional magnetic resonance imaging in essential tremor. Hum Brain Mapp. 2019;40:4686–702. https://doi.org/10.1002/hbm.24730 .
doi: 10.1002/hbm.24730 pubmed: 31332912 pmcid: 6865733
Fang W, Chen H, Wang H, Zhang H, Liu M, Puneet M, Lv F, Cheng O, Wang X, Lu X, Luo T. Multiple Resting-State Networks Are Associated With Tremors and Cognitive Features in Essential Tremor. Mov Disord Off J Mov Disord Soc. 2015;30:1926–36. https://doi.org/10.1002/mds.26375 .
doi: 10.1002/mds.26375
Filion M, Tremblay L. Abnormal spontaneous activity of globus pallidus neurons in monkeys with MPTP-induced parkinsonism. Brain Res. 1991;547:142–51.
pubmed: 1677607
Alamy M, Pons JC, Gambarelli D, Trouche E. A defective control of small-amplitude movements in monkeys with globus pallidus lesions: an experimental study on one component of pallidal bradykinesia. Behav Brain Res. 1995;72:57–62. https://doi.org/10.1016/0166-4328(96)00048-4 .
doi: 10.1016/0166-4328(96)00048-4 pubmed: 8788857
Johnson LA, Aman JE, Yu Y, Escobar Sanabria D, Wang J, Hill M, Dharnipragada R, Patriat R, Fiecas M, Li L, Schrock LE, Cooper SE, Johnson MD, Park MC, Harel N, Vitek JL. High-Frequency Oscillations in the Pallidum A Pathophysiological Biomarker in Parkinson’s Disease? Mov Disord Off J Mov Disord Soc. 2021;36:1332–41. https://doi.org/10.1002/mds.28566 .
doi: 10.1002/mds.28566
Connolly AT, Jensen AL, Bello EM, Netoff TI, Baker KB, Johnson MD, Vitek JL. Modulations in oscillatory frequency and coupling in globus pallidus with increasing parkinsonian severity. J Neurosci Off J Soc Neurosci. 2015;35:6231–40. https://doi.org/10.1523/JNEUROSCI.4137-14.2015 .
doi: 10.1523/JNEUROSCI.4137-14.2015
Obeso JA, Rodríguez-Oroz MC, Benitez-Temino B, Blesa FJ, Guridi J, Marin C, Rodriguez M. Functional organization of the basal ganglia: therapeutic implications for Parkinson’s disease. Mov Disord Off J Mov Disord Soc. 2008;23(Suppl 3):S548-559. https://doi.org/10.1002/mds.22062 .
doi: 10.1002/mds.22062
Wang L, Lei D, Suo X, Li N, Lu Z, Li J, Peng J, Gong Q, Peng R. Resting-state fMRI study on drug-naive patients of essential tremor with and without head tremor. Sci Rep. 2018;8:10580. https://doi.org/10.1038/s41598-018-28778-z .
doi: 10.1038/s41598-018-28778-z pubmed: 30002390 pmcid: 6043592
Isaias IU, Canesi M, Benti R, Gerundini P, Cilia R, Pezzoli G, Antonini A. Striatal dopamine transporter abnormalities in patients with essential tremor. Nucl Med Commun. 2008;29:349–53. https://doi.org/10.1097/MNM.0b013e3282f4d307 .
doi: 10.1097/MNM.0b013e3282f4d307 pubmed: 18317299
Isaias IU, Marotta G, Hirano S, Canesi M, Benti R, Righini A, Tang C, Cilia R, Pezzoli G, Eidelberg D, Antonini A. Imaging essential tremor. Mov Disord. 2010;25:679–86. https://doi.org/10.1002/mds.22870 .
doi: 10.1002/mds.22870 pubmed: 20437537
Brinker D, Granert O, Gövert F, Tödt I, Baumann A, Zeuner KE, Wolke R, Deuschl G, Becktepe JS. Grey matter correlates of dystonic soft signs in essential tremor. Parkinsonism Relat Disord. 2023;112:105457. https://doi.org/10.1016/j.parkreldis.2023.105457 .
doi: 10.1016/j.parkreldis.2023.105457 pubmed: 37245277
Nieuwhof F, Toni I, Dirkx MF, Gallea C, Vidailhet M, Buijink AWG, van Rootselaar A-F, van de Warrenburg BPC, Helmich RC. Cerebello-thalamic activity drives an abnormal motor network into dystonic tremor. NeuroImage Clin. 2022;33:102919. https://doi.org/10.1016/j.nicl.2021.102919 .
doi: 10.1016/j.nicl.2021.102919 pubmed: 34929584

Auteurs

Massimiliano Passaretti (M)

Department of Human Neurosciences, Sapienza University of Rome, Viale dell'Università, 30, 00185, Rome, Italy.
Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden.

Claudia Piervincenzi (C)

Department of Human Neurosciences, Sapienza University of Rome, Viale dell'Università, 30, 00185, Rome, Italy.

Viola Baione (V)

Department of Medicine, Surgery and Neuroscience, University of Siena, Siena, Italy.

Gabriele Pasqua (G)

Department of Human Neurosciences, Sapienza University of Rome, Viale dell'Università, 30, 00185, Rome, Italy.

Donato Colella (D)

Department of Human Neurosciences, Sapienza University of Rome, Viale dell'Università, 30, 00185, Rome, Italy.

Sara Pietracupa (S)

Department of Human Neurosciences, Sapienza University of Rome, Viale dell'Università, 30, 00185, Rome, Italy.
IRCCS Neuromed, Pozzilli, IS, Italy.

Nikolaos Petsas (N)

Department of Public Health and Infectious Disease, Sapienza University of Rome, Rome, Italy.

Luca Angelini (L)

IRCCS Neuromed, Pozzilli, IS, Italy.

Antonio Cannavacciuolo (A)

IRCCS Neuromed, Pozzilli, IS, Italy.

Giulia Paparella (G)

Department of Human Neurosciences, Sapienza University of Rome, Viale dell'Università, 30, 00185, Rome, Italy.
IRCCS Neuromed, Pozzilli, IS, Italy.

Alfredo Berardelli (A)

Department of Human Neurosciences, Sapienza University of Rome, Viale dell'Università, 30, 00185, Rome, Italy.
IRCCS Neuromed, Pozzilli, IS, Italy.

Patrizia Pantano (P)

Department of Human Neurosciences, Sapienza University of Rome, Viale dell'Università, 30, 00185, Rome, Italy.
IRCCS Neuromed, Pozzilli, IS, Italy.

Matteo Bologna (M)

Department of Human Neurosciences, Sapienza University of Rome, Viale dell'Università, 30, 00185, Rome, Italy. matteo.bologna@uniroma1.it.
IRCCS Neuromed, Pozzilli, IS, Italy. matteo.bologna@uniroma1.it.

Classifications MeSH