Skip to main content
Log in

No reliable gray matter changes in essential tremor

  • Original Article
  • Published:
Neurological Sciences Aims and scope Submit manuscript

Abstract

Background

Voxel-based morphometry (VBM) has been used to study human brain gray matter (GM) alterations in essential tremor (ET) for over one decade. However, the literature revealed heterogeneous findings.

Methods

We therefore conducted a coordinate-based meta-analysis to synthesize the VBM studies to examine which brain regions show the most reliable GM alterations in patients with ET relative to healthy controls.

Results

A total of 16 original VBM studies, comprising 387 patients with ET and 355 healthy controls, were included in this meta-analysis. This quantitative meta-analysis revealed no evidence of robust and reliable alterations in regional brain GM structures in ET. Meta-regression analyses indicate that many moderators (e.g., MR field strength, statistical methodology, age, onset age, gender, illness severity, illness duration, and family history) account for some of the heterogeneity in GM across studies.

Conclusions

High heterogeneity in GM alterations across studies may reflect true heterogeneity in ET regarding the clinic, etiology, and pathology, as well as possibly the VBM methodological variations. Currently, this heterogeneity limits the use of VBM as a reliable tool to distinguish ET from healthy controls. In order to improve reproducibility of VBM results in ET, future research may benefit from increasing the sample size, comprehensively subtyping ET phenotypes, and using well-designed and standardized imaging acquisition and analytical protocols. Furthermore, data sharing should be considered as a high priority.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

AES-SDM:

Anisotropic effect-size signed differential mapping

ET:

Essential tremor

FTM-TRS:

Fahn-Tolosa-Marin Tremor Rating Scale

GM:

Gray matter

MNI:

Montreal Neurological Institute

MRI:

Magnetic resonance imaging

PRISMA:

Preferred Reporting Items for Systematic Reviews and Meta-Analyses

SDM:

Seed-based d Mapping

VBM:

Voxel-based morphometry

References

  1. Louis ED, Ferreira JJ (2010) How common is the most common adult movement disorder? Update on the worldwide prevalence of essential tremor. Mov Disord 25(5):534–541. https://doi.org/10.1002/mds.22838

    Article  PubMed  Google Scholar 

  2. Bhatia KP, Bain P, Bajaj N, Elble RJ, Hallett M, Louis ED, Raethjen J, Stamelou M, Testa CM, Deuschl G (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. https://doi.org/10.1002/mds.27121

    Article  Google Scholar 

  3. Louis ED, Benito-Leon J, Ottman R, Bermejo-Pareja F (2007) A population-based study of mortality in essential tremor. Neurology 69(21):1982–1989. https://doi.org/10.1212/01.wnl.0000279339.87987.d7

    Article  PubMed  Google Scholar 

  4. Hopfner F, Helmich RC (2018) The etiology of essential tremor: genes versus environment. Parkinsonism Relat Disord 46(Suppl 1):S92–s96. https://doi.org/10.1016/j.parkreldis.2017.07.014

    Article  PubMed  Google Scholar 

  5. Louis ED (2018) The evolving definition of essential tremor: what are we dealing with? Parkinsonism Relat Disord 46(Suppl 1):S87–s91. https://doi.org/10.1016/j.parkreldis.2017.07.004

    Article  PubMed  Google Scholar 

  6. Hopfner F, Deuschl G (2018) Is essential tremor a single entity? Eur J Neurol 25(1):71–82. https://doi.org/10.1111/ene.13454

    Article  CAS  PubMed  Google Scholar 

  7. Espay AJ, Lang AE, Erro R, Merola A, Fasano A, Berardelli A, Bhatia KP (2017) Essential pitfalls in “essential” tremor. Mov Disord 32(3):325–331. https://doi.org/10.1002/mds.26919

    Article  PubMed  PubMed Central  Google Scholar 

  8. Jain S, Lo SE, Louis ED (2006) Common misdiagnosis of a common neurological disorder: how are we misdiagnosing essential tremor? Arch Neurol 63(8):1100–1104. https://doi.org/10.1001/archneur.63.8.1100

    Article  PubMed  Google Scholar 

  9. Sharifi S, Nederveen AJ, Booij J, van Rootselaar AF (2014) Neuroimaging essentials in essential tremor: a systematic review. Neuroimage Clin 5:217–231. https://doi.org/10.1016/j.nicl.2014.05.003

    Article  PubMed  PubMed Central  Google Scholar 

  10. Cerasa A, Quattrone A (2016) Linking essential tremor to the cerebellum-neuroimaging evidence. Cerebellum 15(3):263–275. https://doi.org/10.1007/s12311-015-0739-8

    Article  CAS  PubMed  Google Scholar 

  11. Ashburner J, Friston KJ (2000) Voxel-based morphometry--the methods. Neuroimage 11(6 Pt 1):805–821. https://doi.org/10.1006/nimg.2000.0582

    Article  CAS  Google Scholar 

  12. Busatto GF, Diniz BS, Zanetti MV (2008) Voxel-based morphometry in Alzheimer’s disease. Expert Rev Neurother 8(11):1691–1702. https://doi.org/10.1586/14737175.8.11.1691

    Article  PubMed  Google Scholar 

  13. Shao N, Yang J, Li J, Shang HF (2014) Voxelwise meta-analysis of gray matter anomalies in progressive supranuclear palsy and Parkinson’s disease using anatomic likelihood estimation. Front Hum Neurosci 8:63. https://doi.org/10.3389/fnhum.2014.00063

    Article  PubMed  PubMed Central  Google Scholar 

  14. Benito-Leon J, Alvarez-Linera J, Hernandez-Tamames JA, Alonso-Navarro H, Jimenez-Jimenez FJ, Louis ED (2009) Brain structural changes in essential tremor: voxel-based morphometry at 3-tesla. J Neurol Sci 287(1–2):138–142. https://doi.org/10.1016/j.jns.2009.08.037

    Article  PubMed  Google Scholar 

  15. Cameron E, Dyke JP, Hernandez N, Louis ED, Dydak U (2018) Cerebral gray matter volume losses in essential tremor: a case-control study using high resolution tissue probability maps. Parkinsonism Relat Disord 51:85–90. https://doi.org/10.1016/j.parkreldis.2018.03.008

    Article  PubMed  PubMed Central  Google Scholar 

  16. Espay AJ, Maloney T, Vannest J, Norris MM, Eliassen JC, Neefus E, Allendorfer JB, Lang AE, Szaflarski JP (2018) Impaired emotion processing in functional (psychogenic) tremor: a functional magnetic resonance imaging study. Neuroimage Clin 17:179–187. https://doi.org/10.1016/j.nicl.2017.10.020

    Article  PubMed  Google Scholar 

  17. Pelzer EA, Nelles C, Pedrosa DJ, Eggers C, Burghaus L, Melzer C, Tittgemeyer M, Timmermann L (2017) Structural differences in impaired verbal fluency in essential tremor patients compared to healthy controls. Brain Behav 7(7):e00722. https://doi.org/10.1002/brb3.722

    Article  PubMed  PubMed Central  Google Scholar 

  18. Bagepally BS, Bhatt MD, Chandran V, Saini J, Bharath RD, Vasudev MK, Prasad C, Yadav R, Pal PK (2012) Decrease in cerebral and cerebellar gray matter in essential tremor: a voxel-based morphometric analysis under 3T MRI. J Neuroimaging 22(3):275–278. https://doi.org/10.1111/j.1552-6569.2011.00598.x

    Article  PubMed  Google Scholar 

  19. Cerasa A, Nistico R, Salsone M, Bono F, Salvino D, Morelli M, Arabia G, Quattrone A (2014) Neuroanatomical correlates of dystonic tremor: a cross-sectional study. Parkinsonism Relat Disord 20(3):314–317. https://doi.org/10.1016/j.parkreldis.2013.12.007

    Article  PubMed  Google Scholar 

  20. Bhalsing KS, Upadhyay N, Kumar KJ, Saini J, Yadav R, Gupta AK, Pal PK (2014) Association between cortical volume loss and cognitive impairments in essential tremor. Eur J Neurol 21(6):874–883. https://doi.org/10.1111/ene.12399

    Article  CAS  PubMed  Google Scholar 

  21. Gallea C, Popa T, Garcia-Lorenzo D, Valabregue R, Legrand AP, Marais L, Degos B, Hubsch C, Fernandez-Vidal S, Bardinet E, Roze E, Lehericy S, Vidailhet M, Meunier S (2015) Intrinsic signature of essential tremor in the cerebello-frontal network. Brain 138(Pt 10):2920–2933. https://doi.org/10.1093/brain/awv171

    Article  PubMed  PubMed Central  Google Scholar 

  22. Lin CH, Chen CM, Lu MK, Tsai CH, Chiou JC, Liao JR, Duann JR (2013) VBM reveals brain volume differences between Parkinson’s disease and essential tremor patients. Front Hum Neurosci 7:247. https://doi.org/10.3389/fnhum.2013.00247

    Article  PubMed  PubMed Central  Google Scholar 

  23. Cao H, Wang R, Luo X, Li X, Hallett M, Thompson-Westra J, Yang J, Qu Q, Yang X (2018) A voxel-based magnetic resonance imaging morphometric study of cerebral and cerebellar gray matter in patients under 65 years with essential tremor. Med Sci Monit 24:3127–3135. https://doi.org/10.12659/msm.906437

    Article  PubMed  PubMed Central  Google Scholar 

  24. Daniels C, Peller M, Wolff S, Alfke K, Witt K, Gaser C, Jansen O, Siebner HR, Deuschl G (2006) Voxel-based morphometry shows no decreases in cerebellar gray matter volume in essential tremor. Neurology 67(8):1452–1456. https://doi.org/10.1212/01.wnl.0000240130.94408.99

    Article  CAS  PubMed  Google Scholar 

  25. Klein JC, Lorenz B, Kang JS, Baudrexel S, Seifried C, van de Loo S, Steinmetz H, Deichmann R, Hilker R (2011) Diffusion tensor imaging of white matter involvement in essential tremor. Hum Brain Mapp 32(6):896–904. https://doi.org/10.1002/hbm.21077

    Article  PubMed  Google Scholar 

  26. Fang W, Lv F, Luo T, Cheng O, Liao W, Sheng K, Wang X, Wu F, Hu Y, Luo J, Yang QX, Zhang H (2013) Abnormal regional homogeneity in patients with essential tremor revealed by resting-state functional MRI. PLoS One 8(7):e69199. https://doi.org/10.1371/journal.pone.0069199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Nicoletti V, Cecchi P, Frosini D, Pesaresi I, Fabbri S, Diciotti S, Bonuccelli U, Cosottini M, Ceravolo R (2015) Morphometric and functional MRI changes in essential tremor with and without resting tremor. J Neurol 262(3):719–728. https://doi.org/10.1007/s00415-014-7626-y

    Article  PubMed  Google Scholar 

  28. Buijink AW, Broersma M, van der Stouwe AM, Sharifi S, Tijssen MA, Speelman JD, Maurits NM, van Rootselaar AF (2016) Cerebellar atrophy in cortical myoclonic tremor and not in hereditary essential tremor-a voxel-based morphometry study. Cerebellum (London, England) 15(6):696–704. https://doi.org/10.1007/s12311-015-0734-0

    Article  CAS  Google Scholar 

  29. Fang W, Chen H, Wang H, Zhang H, Puneet M, Liu M, Lv F, Luo T, Cheng O, Wang X, Lu X (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. https://doi.org/10.1002/hbm.23024

    Article  PubMed  Google Scholar 

  30. Archer DB, Coombes SA, Chu WT, Chung JW, Burciu RG, Okun MS, Wagle Shukla A, Vaillancourt DE (2018) A widespread visually-sensitive functional network relates to symptoms in essential tremor. Brain 141(2):472–485. https://doi.org/10.1093/brain/awx338

    Article  PubMed  Google Scholar 

  31. Quattrone A, Cerasa A, Messina D, Nicoletti G, Hagberg GE, Lemieux L, Novellino F, Lanza P, Arabia G, Salsone M (2008) Essential head tremor is associated with cerebellar vermis atrophy: a volumetric and voxel-based morphometry MR imaging study. Am J Neuroradiol 29(9):1692–1697. https://doi.org/10.3174/ajnr.A1190

    Article  CAS  PubMed  Google Scholar 

  32. Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med 151(4):264–269

    Article  Google Scholar 

  33. Louis ED, Ford B, Lee H, Andrews H, Cameron G (1998) Diagnostic criteria for essential tremor: a population perspective. Arch Neurol 55(6):823–828

    Article  CAS  Google Scholar 

  34. Chouinard S, Louis ED, Fahn S (1997) Agreement among movement disorder specialists on the clinical diagnosis of essential tremor. Mov Disord 12(6):973–976. https://doi.org/10.1002/mds.870120621

    Article  CAS  PubMed  Google Scholar 

  35. Louis ED, Ford B, Frucht S, Barnes LF, M XT, Ottman R (2001) Risk of tremor and impairment from tremor in relatives of patients with essential tremor: a community-based family study. Ann Neurol 49(6):761–769

    Article  CAS  Google Scholar 

  36. Deuschl G, Bain P, Brin M (1998) Consensus statement of the movement disorder society on tremor. Ad Hoc Scientific Committee. Mov Disord 13(Suppl 3):2–23

    PubMed  Google Scholar 

  37. Bain P, Brin M, Deuschl G, Elble R, Jankovic J, Findley L, Koller WC, Pahwa R (2000) Criteria for the diagnosis of essential tremor. Neurology 54(11 Suppl 4):S7

    CAS  PubMed  Google Scholar 

  38. Chen ZQ, Du MY, Zhao YJ, Huang XQ, Li J, Lui S, Hu JM, Sun HQ, Liu J, Kemp GJ, Gong QY (2015) Voxel-wise meta-analyses of brain blood flow and local synchrony abnormalities in medication-free patients with major depressive disorder. J Psychiatry Neurosci 40(6):401–411

    Article  Google Scholar 

  39. Pan P, Liu Y, Zhang Y, Zhao H, Ye X, Xu Y (2017) Brain gray matter abnormalities in progressive supranuclear palsy revisited. Oncotarget 8(46):80941–80955. https://doi.org/10.18632/oncotarget.20895

    Article  PubMed  PubMed Central  Google Scholar 

  40. Albajes-Eizagirre A, Radua J (2018) What do results from coordinate-based meta-analyses tell us? Neuroimage 176:550–553. https://doi.org/10.1016/j.neuroimage.2018.04.065

    Article  PubMed  Google Scholar 

  41. Rogers JC, De Brito SA (2016) Cortical and subcortical gray matter volume in youths with conduct problems: a meta-analysis. JAMA Psychiatry 73(1):64–72. https://doi.org/10.1001/jamapsychiatry.2015.2423

    Article  Google Scholar 

  42. Kronbichler L, Tschernegg M, Martin AI, Schurz M, Kronbichler M (2017) Abnormal brain activation during theory of mind tasks in schizophrenia: a meta-analysis. Schizophr Bull 43(6):1240–1250. https://doi.org/10.1093/schbul/sbx073

    Article  PubMed  PubMed Central  Google Scholar 

  43. Ma HR, Sheng LQ, Pan PL, Wang GD, Luo R, Shi HC, Dai ZY, Zhong JG (2018) Cerebral glucose metabolic prediction from amnestic mild cognitive impairment to Alzheimer’s dementia: a meta-analysis. Transl Neurodegener 7:9. https://doi.org/10.1186/s40035-018-0114-z

    Article  PubMed  PubMed Central  Google Scholar 

  44. Alegria AA, Radua J, Rubia K (2016) Meta-analysis of fMRI studies of disruptive behavior disorders. Am J Psychiatry 173(11):1119–1130. https://doi.org/10.1176/appi.ajp.2016.15081089

    Article  PubMed  Google Scholar 

  45. Radua J, Mataix-Cols D, Phillips ML, El-Hage W, Kronhaus DM, Cardoner N, Surguladze S (2012) A new meta-analytic method for neuroimaging studies that combines reported peak coordinates and statistical parametric maps. Eur Psychiatry 27(8):605–611. https://doi.org/10.1016/j.eurpsy.2011.04.001

    Article  CAS  PubMed  Google Scholar 

  46. Radua J, Rubia K, Canales-Rodriguez EJ, Pomarol-Clotet E, Fusar-Poli P, Mataix-Cols D (2014) Anisotropic kernels for coordinate-based meta-analyses of neuroimaging studies. Front Psychiatry 5:13. https://doi.org/10.3389/fpsyt.2014.00013

    Article  PubMed  PubMed Central  Google Scholar 

  47. Wise T, Radua J, Nortje G, Cleare AJ, Young AH, Arnone D (2016) Voxel-based meta-analytical evidence of structural disconnectivity in major depression and bipolar disorder. Biol Psychiatry 79(4):293–302. https://doi.org/10.1016/j.biopsych.2015.03.004

    Article  PubMed  Google Scholar 

  48. Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634

    Article  CAS  Google Scholar 

  49. Teive HA (2012) Essential tremor: phenotypes. Parkinsonism Relat Disord 18(Suppl 1):S140–S142. https://doi.org/10.1016/s1353-8020(11)70044-x

    Article  PubMed  Google Scholar 

  50. Louis ED (2016) Non-motor symptoms in essential tremor: a review of the current data and state of the field. Parkinsonism Relat Disord 22(Suppl 1):S115–S118. https://doi.org/10.1016/j.parkreldis.2015.08.034

    Article  PubMed  Google Scholar 

  51. Lee SM, Kim M, Lee HM, Kwon KY, Koh SB (2015) Nonmotor symptoms in essential tremor: comparison with Parkinson's disease and normal control. J Neurol Sci 349(1–2):168–173. https://doi.org/10.1016/j.jns.2015.01.012

    Article  PubMed  Google Scholar 

  52. Wu Y, Wang X, Wang C, Sun Q, Song N, Zhou Y, Jiang Q, Qiao Y, Xu J, Liang L, Tang H, Ma J, Gao X, Chen SD (2016) Prevalence and clinical features of non-motor symptoms of essential tremor in Shanghai rural area. Parkinsonism Relat Disord 22:15–20. https://doi.org/10.1016/j.parkreldis.2015.10.617

    Article  PubMed  Google Scholar 

  53. Chunling W, Zheng X (2016) Review on clinical update of essential tremor. Neurol Sci 37(4):495–502. https://doi.org/10.1007/s10072-015-2380-1

    Article  PubMed  Google Scholar 

  54. Louis ED (2018) Essential tremor then and now: how views of the most common tremor diathesis have changed over time. Parkinsonism Relat Disord 46(Suppl 1):S70–s74. https://doi.org/10.1016/j.parkreldis.2017.07.010

    Article  PubMed  Google Scholar 

  55. Symanski C, Shill HA, Dugger B, Hentz JG, Adler CH, Jacobson SA, Driver-Dunckley E, Beach TG (2014) Essential tremor is not associated with cerebellar Purkinje cell loss. Mov Disord 29(4):496–500. https://doi.org/10.1002/mds.25845

    Article  PubMed  Google Scholar 

  56. Lin CY, Louis ED, Faust PL, Koeppen AH, Vonsattel JP, Kuo SH (2014) Abnormal climbing fibre-Purkinje cell synaptic connections in the essential tremor cerebellum. Brain 137(Pt 12):3149–3159. https://doi.org/10.1093/brain/awu281

    Article  PubMed  PubMed Central  Google Scholar 

  57. Axelrad JE, Louis ED, Honig LS, Flores I, Ross GW, Pahwa R, Lyons KE, Faust PL, Vonsattel JP (2008) Reduced Purkinje cell number in essential tremor: a postmortem study. Arch Neurol 65(1):101–107. https://doi.org/10.1001/archneurol.2007.8

    Article  PubMed  PubMed Central  Google Scholar 

  58. Louis ED, Faust PL, Vonsattel JP, Honig LS, Rajput A, Robinson CA, Rajput A, Pahwa R, Lyons KE, Ross GW, Borden S, Moskowitz CB, Lawton A, Hernandez N (2007) Neuropathological changes in essential tremor: 33 cases compared with 21 controls. Brain 130(Pt 12):3297–3307. https://doi.org/10.1093/brain/awm266

    Article  PubMed  Google Scholar 

  59. Kuo SH, Erickson-Davis C, Gillman A, Faust PL, Vonsattel JP, Louis ED (2011) Increased number of heterotopic Purkinje cells in essential tremor. J Neurol Neurosurg Psychiatry 82(9):1038–1040. https://doi.org/10.1136/jnnp.2010.213330

    Article  PubMed  Google Scholar 

  60. Louis ED, Babij R, Lee M, Cortes E, Vonsattel JP (2013) Quantification of cerebellar hemispheric Purkinje cell linear density: 32 ET cases versus 16 controls. Mov Disord 28(13):1854–1859. https://doi.org/10.1002/mds.25629

    Article  PubMed  Google Scholar 

  61. Rajput AH, Robinson CA, Rajput ML, Rajput A (2011) Cerebellar Purkinje cell loss is not pathognomonic of essential tremor. Parkinsonism Relat Disord 17(1):16–21. https://doi.org/10.1016/j.parkreldis.2010.08.009

    Article  CAS  PubMed  Google Scholar 

  62. Rajput AH, Robinson CA, Rajput ML, Robinson SL, Rajput A (2012) Essential tremor is not dependent upon cerebellar Purkinje cell loss. Parkinsonism Relat Disord 18(5):626–628. https://doi.org/10.1016/j.parkreldis.2012.01.013

    Article  CAS  PubMed  Google Scholar 

  63. Button KS, Ioannidis JP, Mokrysz C, Nosek BA, Flint J, Robinson ES, Munafo MR (2013) Power failure: why small sample size undermines the reliability of neuroscience. Nat Rev Neurosci 14(5):365–376. https://doi.org/10.1038/nrn3475

    Article  CAS  Google Scholar 

  64. Fusar-Poli P, Radua J, Frascarelli M, Mechelli A, Borgwardt S, Di Fabio F, Biondi M, Ioannidis JP, David SP (2014) Evidence of reporting biases in voxel-based morphometry (VBM) studies of psychiatric and neurological disorders. Hum Brain Mapp 35(7):3052–3065. https://doi.org/10.1002/hbm.22384

    Article  PubMed  Google Scholar 

  65. Borghi JA, Van Gulick AE (2018) Data management and sharing in neuroimaging: practices and perceptions of MRI researchers. PLoS One 13(7):e0200562. https://doi.org/10.1371/journal.pone.0200562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Breeze JL, Poline JB, Kennedy DN (2012) Data sharing and publishing in the field of neuroimaging. Gigascience 1(1):9. https://doi.org/10.1186/2047-217x-1-9

    Article  PubMed  PubMed Central  Google Scholar 

  67. Celle S, Delon-Martin C, Roche F, Barthelemy JC, Pepin JL, Dojat M (2016) Desperately seeking grey matter volume changes in sleep apnea: a methodological review of magnetic resonance brain voxel-based morphometry studies. Sleep Med Rev 25:112–120. https://doi.org/10.1016/j.smrv.2015.03.001

    Article  PubMed  Google Scholar 

  68. Scott-Wittenborn N, Karadaghy OA, Piccirillo JF, Peelle JE (2017) A methodological assessment of studies that use voxel-based morphometry to study neural changes in tinnitus patients. Hear Res 355:23–32. https://doi.org/10.1016/j.heares.2017.09.002

    Article  PubMed  PubMed Central  Google Scholar 

  69. Ridgway GR, Henley SM, Rohrer JD, Scahill RI, Warren JD, Fox NC (2008) Ten simple rules for reporting voxel-based morphometry studies. Neuroimage 40(4):1429–1435. https://doi.org/10.1016/j.neuroimage.2008.01.003

    Article  PubMed  Google Scholar 

  70. Han Q, Hou Y, Shang H (2018) A voxel-wise meta-analysis of gray matter abnormalities in essential tremor. Front Neurol 9:495. https://doi.org/10.3389/fneur.2018.00495

    Article  PubMed  PubMed Central  Google Scholar 

  71. Eickhoff SB, Nichols TE, Laird AR, Hoffstaedter F, Amunts K, Fox PT, Bzdok D, Eickhoff CR (2016) Behavior, sensitivity, and power of activation likelihood estimation characterized by massive empirical simulation. Neuroimage 137:70–85. https://doi.org/10.1016/j.neuroimage.2016.04.072

    Article  PubMed  PubMed Central  Google Scholar 

  72. Radua J, Mataix-Cols D (2012) Meta-analytic methods for neuroimaging data explained. Biol Mood Anxiety Disord 2:6. https://doi.org/10.1186/2045-5380-2-6

    Article  PubMed  PubMed Central  Google Scholar 

  73. Book GA, Stevens MC, Assaf M, Glahn DC, Pearlson GD (2016) Neuroimaging data sharing on the neuroinformatics database platform. Neuroimage 124(Pt B):1089–1092. https://doi.org/10.1016/j.neuroimage.2015.04.022

    Article  PubMed  Google Scholar 

  74. Nichols TE, Das S, Eickhoff SB, Evans AC, Glatard T, Hanke M, Kriegeskorte N, Milham MP, Poldrack RA, Poline JB, Proal E, Thirion B, Van Essen DC, White T, Yeo BT (2017) Best practices in data analysis and sharing in neuroimaging using MRI. Nat Neurosci 20(3):299–303. https://doi.org/10.1038/nn.4500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Mennes M, Biswal BB, Castellanos FX, Milham MP (2013) Making data sharing work: the FCP/INDI experience. Neuroimage 82:683–691. https://doi.org/10.1016/j.neuroimage.2012.10.064

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank all the authors of the included studies.

Funding

This work was supported by the National Natural Science Foundation of China (81630028, 81601161), the Key Research and Development Program of Jiangsu Province of China (BE2016610), the National Key Research and Development Program of China (2016YFC1300504), and the Jiangsu Province Key Medical Discipline (ZDXKA2016020).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Yun Xu or Ling Chen.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 28 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Luo, R., Pan, P., Xu, Y. et al. No reliable gray matter changes in essential tremor. Neurol Sci 40, 2051–2063 (2019). https://doi.org/10.1007/s10072-019-03933-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10072-019-03933-0

Keywords

Navigation