Differential patterns of functional connectivity in tremor dominant Parkinson's disease and essential tremor plus.
ETP
Functional connectivity
Seed-to-voxel
TDPD
Journal
Journal of neural transmission (Vienna, Austria : 1996)
ISSN: 1435-1463
Titre abrégé: J Neural Transm (Vienna)
Pays: Austria
ID NLM: 9702341
Informations de publication
Date de publication:
02 Mar 2024
02 Mar 2024
Historique:
received:
27
12
2023
accepted:
23
02
2024
medline:
2
3
2024
pubmed:
2
3
2024
entrez:
2
3
2024
Statut:
aheadofprint
Résumé
Tremor dominant Parkinson's disease (TDPD) and essential tremor plus (ETP) syndrome are commonly encountered tremor dominant neurological disorders. Although the basal ganglia thalamocortical (BGTC) and cerebello thalamocortical (CTC) networks are implicated in tremorogenesis, the extent of functional connectivity alterations across disorders is uncertain. This study aims to evaluate functional connectivity of the BGTC and CTC in TDPD and ETP. Resting state functional MRI was acquired for 25 patients with TDPD, ETP and 22 healthy controls (HC). Following pre-processing and denoising, seed-to-voxel based connectivity was carried out at FDR < 0.05 using ROIs belonging to the BGTC and CTC. Fahn-Tolosa-Marin tremor rating scale (FTMRS) was correlated with the average connectivity values at FDR < 0.05. Compared to HC, TDPD showed decreased connectivity between cerebellum and pre, post central gyrus. While, ETP showed decreased connectivity between pallidum and occipital cortex, precuneus, cuneus compared to HC. In comparison to ETP, TDPD showed increased connectivity between precentral gyrus, pallidum, SNc with the default mode network (DMN), and decreased connectivity between cerebellum with superior, middle frontal gyrus was observed. Tremor severity positively correlated with connectivity between SNc and DMN in TDPD, and negatively correlated with pallidal connectivity in ETP. Pattern of BGTC, CTC involvement is differential i.e., higher connectivity of the BGTC nodes in TDPD, and higher connectivity of cerebellar nodes in ETP. The interesting observation of pallidal involvement in ETP suggests the role of BGTC in the pathogenesis of ETP, and indicated similarities in concepts of tremor genesis in TDPD and ETP.
Identifiants
pubmed: 38430265
doi: 10.1007/s00702-024-02761-7
pii: 10.1007/s00702-024-02761-7
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Department of Biotechnology, Ministry of Science and Technology, India
ID : BT/PR27340/MED/122/130/2018
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Austria, part of Springer Nature.
Références
Andersson JL, Hutton C, Ashburner J, Turner R, Friston K (2001) Modeling geometric deformations in EPI time series. NeuroImage 13(5):903–919
pubmed: 11304086
doi: 10.1006/nimg.2001.0746
Archer DB, Coombes SA, Chu WT et al (2018) A widespread visually-sensitive functional network relates to symptoms in essential tremor. Brain 141(2):472–485
pubmed: 29293948
doi: 10.1093/brain/awx338
Ashburner J, Friston KJ (2005) Unified segmentation. NeuroImage 26(3):839–851
pubmed: 15955494
doi: 10.1016/j.neuroimage.2005.02.018
Basit H, Kahwaji CI (2020) Clonazepam
Benabid AL, Pollak P, Gervason C et al (1991) Long-term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus. Lancet 337(8738):403–406
pubmed: 1671433
doi: 10.1016/0140-6736(91)91175-T
Benabid AL, Pollak P, Gao D et al (1996) Chronic electrical stimulation of the ventralis intermedius nucleus of the thalamus as a treatment of movement disorders. J Neurosurg 84(2):203–214
pubmed: 8592222
doi: 10.3171/jns.1996.84.2.0203
Benito-León J, Louis ED, Romero JP et al (2015) Altered functional connectivity in essential tremor: a resting-state fMRI study. Medicine. ;94(49)
Benito-León J, Sanz‐Morales E, Melero H et al (2019) Graph theory analysis of resting‐state functional magnetic resonance imaging in essential tremor. Hum Brain Mapp
Bergman H, Feingold A, Nini A et al (1998) Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates. Trends Neurosci 21(1):32–38
pubmed: 9464684
doi: 10.1016/S0166-2236(97)01151-X
Bhatia KP, Bain P, Bajaj N et al (2018) Consensus Statement on the classification of tremors. From the task force on tremor of the International Parkinson and Movement Disorder Society. Mov Disord 33(1):75–87
pubmed: 29193359
doi: 10.1002/mds.27121
Brittain J-S, Brown P (2013) The many roads to tremor. Exp Neurol 250:104–107
pubmed: 24070853
doi: 10.1016/j.expneurol.2013.09.012
Bucher SF, Seelos KC, Dodel RC, Reiser M, Oertel WH (1997) Activation mapping in essential tremor with functional magnetic resonance imaging. Annals Neurology: Official J Am Neurol Association Child Neurol Soc 41(1):32–40
doi: 10.1002/ana.410410108
Buijink AW, Broersma M, van der Stouwe AM et al (2015) Rhythmic finger tapping reveals cerebellar dysfunction in essential tremor. Parkinsonism Relat Disord 21(4):383–388
pubmed: 25703340
doi: 10.1016/j.parkreldis.2015.02.003
Cagnan H, Little S, Foltynie T et al (2014) The nature of tremor circuits in parkinsonian and essential tremor. Brain 137(Pt 12):3223–3234
pubmed: 25200741
pmcid: 4240284
doi: 10.1093/brain/awu250
Caligiuri ME, Arabia G, Barbagallo G et al (2017) Structural connectivity differences in essential tremor with and without resting tremor. J Neurol 264(9):1865–1874
pubmed: 28730570
doi: 10.1007/s00415-017-8553-5
Defer GL, Widner H, Marié RM, Rémy P, Levivier M (1999) Core assessment program for surgical interventional therapies in Parkinson’s disease (CAPSIT-PD). Mov Disord 14(4):572–584
pubmed: 10435493
doi: 10.1002/1531-8257(199907)14:4<572::AID-MDS1005>3.0.CO;2-C
Desikan RS, Ségonne F, Fischl B et al (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 31(3):968–980
pubmed: 16530430
doi: 10.1016/j.neuroimage.2006.01.021
Dirkx MF, den Ouden H, Aarts E et al (2016) The Cerebral Network of Parkinson’s Tremor: an effective connectivity fMRI study. J Neurosci 36(19):5362–5372
pubmed: 27170132
pmcid: 6601802
doi: 10.1523/JNEUROSCI.3634-15.2016
Dirkx MF, den Ouden HE, Aarts E et al (2017) Dopamine controls Parkinson’s tremor by inhibiting the cerebellar thalamus. Brain 140(3):721–734
pubmed: 28073788
Dupuis MJ, Evrard FL, Jacquerye PG, Picard GR, Lermen OG (2010) Disappearance of essential tremor after stroke. Mov Disord 25(16):2884–2887
pubmed: 20836089
doi: 10.1002/mds.23328
Elble RJ (1996) Central mechanisms of tremor. J Clin Neurophysiol 13(2):133–144
pubmed: 8849968
doi: 10.1097/00004691-199603000-00004
Fahn S, Tolosa E, Marín C (1993) Clinical rating scale for tremor. Parkinson’s Disease Mov Disorders Baltimore: Williams Wilkins. :271–280
Fang W, Lv F, Luo T et al (2013) Abnormal regional homogeneity in patients with essential tremor revealed by resting-state functional MRI. PLoS ONE 8(7):e69199
pubmed: 23869236
pmcid: 3711903
doi: 10.1371/journal.pone.0069199
Fang W, Chen H, Wang H et al (2015) Multiple resting-state networks are Associated with tremors and cognitive features in essential tremor. Mov Disord 30(14):1926–1936
pubmed: 26407908
doi: 10.1002/mds.26375
Fang W, Chen H, Wang H et al (2016) Essential tremor is associated with disruption of functional connectivity in the ventral intermediate nucleus—motor cortex—cerebellum circuit. Hum Brain Mapp 37(1):165–178
pubmed: 26467643
doi: 10.1002/hbm.23024
Gallea C, Popa T, García-Lorenzo D et al (2015) Intrinsic signature of essential tremor in the cerebello-frontal network. Brain 138(10):2920–2933
pubmed: 26115677
pmcid: 4747645
doi: 10.1093/brain/awv171
Gibson WS, Jo HJ, Testini P et al (2016) Functional correlates of the therapeutic and adverse effects evoked by thalamic stimulation for essential tremor. Brain 139(8):2198–2210
pubmed: 27329768
pmcid: 4958905
doi: 10.1093/brain/aww145
Grimaldi G, Manto M (2013) Is essential tremor a Purkinjopathy? The role of the cerebellar cortex in its pathogenesis. Mov Disord 28(13):1759–1761
pubmed: 24114851
doi: 10.1002/mds.25645
Helmich RC (2017) The cerebral basis of parkinsonian tremor: a network perspective. Mov Disord
Helmich RC, Janssen MJ, Oyen WJ, Bloem BR, Toni I (2011) Pallidal dysfunction drives a cerebellothalamic circuit into Parkinson tremor. Ann Neurol 69(2):269–281
pubmed: 21387372
doi: 10.1002/ana.22361
Helmich RC, Toni I, Deuschl G, Bloem BR (2013) The pathophysiology of essential tremor and Parkinson’s tremor. Curr Neurol Neurosci Rep 13(9):378
pubmed: 23893097
doi: 10.1007/s11910-013-0378-8
Henson R, Buechel C, Josephs O, Friston K (1999) The slice-timing problem in event-related fMRI. NeuroImage 9:125
Hirsch EC, Mouatt A, Faucheux B et al (1992) Dopamine, tremor, and Parkinson’s disease. Lancet 340(8811):125–126
pubmed: 1352004
doi: 10.1016/0140-6736(92)90457-E
Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55(3):181–184
pubmed: 1564476
pmcid: 1014720
doi: 10.1136/jnnp.55.3.181
Jang C, Park H-J, Chang WS, Pae C, Chang JW (2016) Immediate and longitudinal alterations of functional networks after thalamotomy in essential tremor. Front Neurol 7:184
pubmed: 27822200
pmcid: 5076435
doi: 10.3389/fneur.2016.00184
Jankovic J, McDermott M, Carter J et al (1990) Variable expression of Parkinson’s disease: a base-line analysis of the DATATOP cohort. The Parkinson Study Group. Neurology 40(10):1529–1534
pubmed: 2215943
doi: 10.1212/WNL.40.10.1529
Lenka A, Bhalsing KS, Panda R et al (2017) Role of altered cerebello-thalamo-cortical network in the neurobiology of essential tremor. Neuroradiology 59(2):157–168
pubmed: 28062908
doi: 10.1007/s00234-016-1771-1
Li J-y, Lu Z-j, Suo X-l et al (2020a) Patterns of intrinsic brain activity in essential tremor with resting tremor and tremor-dominant Parkinson’s disease. Brain Imaging Behav 14:2606–2617
pubmed: 31989422
doi: 10.1007/s11682-019-00214-4
Li J-y, Lu Z-j, Suo X-l et al (2020b) Patterns of intrinsic brain activity in essential tremor with resting tremor and tremor-dominant Parkinson’s disease. Brain Imaging Behav 14(6):2606–2617
pubmed: 31989422
doi: 10.1007/s11682-019-00214-4
Li J-y, Suo X-l, Li N-n et al (2021) Altered spontaneous brain activity in essential tremor with and without resting tremor: a resting-state fMRI study. Magn Reson Mater Phys Biol Med 34(2):201–212
doi: 10.1007/s10334-020-00865-1
Lin CH, Chen CM, Lu MK et al (2013) VBM reveals brain volume differences between Parkinson’s Disease and essential Tremor patients. Front Hum Neurosci 7:247
pubmed: 23785322
pmcid: 3682128
doi: 10.3389/fnhum.2013.00247
Louis ED, Huey ED, Cosentino S (2021) Features of ET plus correlate with age and tremor duration:ET plus may be a disease stage rather than a subtype of essential tremor. Parkinsonism Relat Disord 91:42–47
pubmed: 34482193
doi: 10.1016/j.parkreldis.2021.08.017
McAuley J, Marsden C (2000) Physiological and pathological tremors and rhythmic central motor control. Brain 123(8):1545–1567
pubmed: 10908186
doi: 10.1093/brain/123.8.1545
Middlebrooks EH, Okromelidze L, Wong JK et al (2021) Connectivity correlates to predict essential tremor deep brain stimulation outcome: evidence for a common treatment pathway. NeuroImage: Clin 32:102846
pubmed: 34624639
doi: 10.1016/j.nicl.2021.102846
Mueller K, Jech R, Hoskovcová M et al (2017) General and selective brain connectivity alterations in essential tremor: a resting state fMRI study. NeuroImage: Clin 16:468–476
pubmed: 28913163
doi: 10.1016/j.nicl.2017.06.004
Muthuraman M, Heute U, Arning K et al (2012) Oscillating central motor networks in pathological tremors and voluntary movements. What Makes Difference? Neuroimage 60(2):1331–1339
pubmed: 22293134
Nicoletti V, Cecchi P, Frosini D et al (2015) Morphometric and functional MRI changes in essential tremor with and without resting tremor. J Neurol 262(3):719–728
pubmed: 25572161
doi: 10.1007/s00415-014-7626-y
Nicoletti V, Cecchi P, Pesaresi I, Frosini D, Cosottini M, Ceravolo R (2020) Cerebello-Thalamo-cortical network is intrinsically altered in essential tremor: evidence from a resting state functional MRI study. Sci Rep 10(1):1–8
doi: 10.1038/s41598-020-73714-9
Nieuwhof F, Toni I, Dirkx MF et al (2022) Cerebello-thalamic activity drives an abnormal motor network into dystonic tremor. NeuroImage: Clin 33:102919
pubmed: 34929584
doi: 10.1016/j.nicl.2021.102919
Novellino F, Nicoletti G, Cherubini A et al (2016) Cerebellar involvement in essential tremor with and without resting tremor: a diffusion Tensor Imaging study. Parkinsonism Relat Disord 27:61–66
pubmed: 27050442
doi: 10.1016/j.parkreldis.2016.03.022
Ohye C, Hirai T, Miyazaki M, Shibazaki T, Nakajima H (1982) Vim thalamotomy for the treatment of various kinds of tremor. Stereotact Funct Neurosurg 45(3):275–280
doi: 10.1159/000101611
Passamonti L, Novellino F, Cerasa A et al (2011) Altered cortical-cerebellar circuits during verbal working memory in essential tremor. Brain 134(Pt 8):2274–2286
pubmed: 21747127
doi: 10.1093/brain/awr164
Prasad S, Rastogi B, Shah A et al (2018) DTI in essential tremor with and without rest tremor: two sides of the same coin? Mov Disord
Raethjen J, Deuschl G (2012) The oscillating central network of essential tremor. Clin Neurophysiol 123(1):61–64
pubmed: 22055842
doi: 10.1016/j.clinph.2011.09.024
Safai A, Prasad S, Chougule T, Saini J, Pal PK, Ingalhalikar M (2020) Microstructural abnormalities of substantia nigra in Parkinson’s disease: a neuromelanin sensitive MRI atlas based study. Hum Brain Mapp 41(5):1323–1333
pubmed: 31778276
doi: 10.1002/hbm.24878
Saranza G, Lang AE (2021) Levodopa challenge test: indications, protocol, and guide. J Neurol 268(9):3135–3143
pubmed: 32333167
doi: 10.1007/s00415-020-09810-7
Schnitzler A, Gross J (2005) Normal and pathological oscillatory communication in the brain. Nat Rev Neurosci 6(4):285–296
pubmed: 15803160
doi: 10.1038/nrn1650
Schnitzler A, Munks C, Butz M, Timmermann L, Gross J (2009) Synchronized brain network associated with essential tremor as revealed by magnetoencephalography. Mov Disord 24(11):1629–1635
pubmed: 19514010
doi: 10.1002/mds.22633
Shahrokhi M, Gupta V, Propranolol (2020)
Tikoo S, Pietracupa S, Tommasin S et al (2020) Functional disconnection of the dentate nucleus in essential tremor. J Neurol. :1–10
Timmermann L, Gross J, Dirks M, Volkmann J, Freund HJ, Schnitzler A (2003) The cerebral oscillatory network of parkinsonian resting tremor. Brain 126(Pt 1):199–212
pubmed: 12477707
doi: 10.1093/brain/awg022
Tzourio-Mazoyer N, Landeau B, Papathanassiou D et al (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15(1):273–289
pubmed: 11771995
doi: 10.1006/nimg.2001.0978
van den Berg KR, Helmich RC (2021) The role of the Cerebellum in Tremor–evidence from Neuroimaging. Tremor Other Hyperkinetic Movements. ;11
Whitfield-Gabrieli S, Nieto-Castanon A (2012) Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect 2(3):125–141
pubmed: 22642651
doi: 10.1089/brain.2012.0073
Yin W, Lin W, Li W, Qian S, Mou X (2016) Resting state fMRI demonstrates a disturbance of the Cerebello-Cortical Circuit in essential tremor. Brain Topogr 29(3):412–418
pubmed: 26868003
doi: 10.1007/s10548-016-0474-6