Skip to main content
SpringerLink
Log in

Combined brain topological metrics with machine learning to distinguish essential tremor and tremor-dominant Parkinson’s disease

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

Abstract

Background

Essential tremor (ET) and Parkinson’s disease (PD) are the two most prevalent movement disorders, sharing several overlapping tremor clinical features. Although growing evidence pointed out that changes in similar brain network nodes are associated with these two diseases, the brain network topological properties are still not very clear.

Objective

The combination of graph theory analysis with machine learning (ML) algorithms provides a promising way to reveal the topological pathogenesis in ET and tremor-dominant PD (tPD).

Methods

Topological metrics were extracted from Resting-state functional images of 86 ET patients, 86 tPD patients, and 86 age- and sex-matched healthy controls (HCs). Three steps were conducted to feature dimensionality reduction and four frequently used classifiers were adopted to discriminate ET, tPD, and HCs.

Results

A support vector machine classifier achieved the best classification performance of four classifiers for discriminating ET, tPD, and HCs with 89.0% mean accuracy (mACC) and was used for binary classification. Particularly, the binary classification performances among ET vs. tPD, ET vs. HCs, and tPD vs. HCs were with 94.2% mACC, 86.0% mACC, and 86.3% mACC, respectively. The most power discriminative features were mainly located in the default, frontal-parietal, cingulo-opercular, sensorimotor, and cerebellum networks. Correlation analysis results showed that 2 topological features negatively and 1 positively correlated with clinical characteristics.

Conclusions

These results demonstrated that combining topological metrics with ML algorithms could not only achieve high classification accuracy for discrimination ET, tPD, and HCs but also help to reveal the potential brain topological network pathogenesis in ET and tPD.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

The data supporting the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.

References

  1. Louis ED (2016) Diagnosis and management of tremor. Continuum (Minneapolis, Minn.) 22:1143–1158

    PubMed  Google Scholar 

  2. Algarni M, Fasano A (2018) The overlap between essential tremor and Parkinson disease. Parkinsonism Relat Disord 46(Suppl 1):S101–S104

    Article  PubMed  Google Scholar 

  3. Thenganatt MA, Jankovic J (2016) The relationship between essential tremor and Parkinson’s disease. Parkinsonism Relat Disord 22(Suppl 1):S162–S165

    Article  PubMed  Google Scholar 

  4. Tarakad A, Jankovic J (2018) Essential tremor and Parkinson’s disease: exploring the relationship. Tremor Other Hyperkinetic Mov (New York, N.Y.) 8:589

    Article  Google Scholar 

  5. 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 10:16661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Wu T, Hallett M (2013) The cerebellum in Parkinson’s disease. Brain : J Neurol 136:696–709

    Article  Google Scholar 

  7. Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52:1059–1069

    Article  PubMed  Google Scholar 

  8. Liao X, Vasilakos AV, He Y (2017) Small-world human brain networks: perspectives and challenges. Neurosci Biobehav Rev 77:286–300

    Article  PubMed  Google Scholar 

  9. Benito-León J, Sanz-Morales E, Melero H, Louis ED, Romero JP, Rocon E, Malpica N (2019) Graph theory analysis of resting-state functional magnetic resonance imaging in essential tremor. Hum Brain Mapp 40:4686–4702

    Article  PubMed  PubMed Central  Google Scholar 

  10. Novaes NP, Balardin JB, Hirata FC, Melo L, Amaro E Jr, Barbosa ER, Sato JR, Cardoso EF (2021) Global efficiency of the motor network is decreased in Parkinson’s disease in comparison with essential tremor and healthy controls. Brain Behav 11:e02178

    Article  PubMed  PubMed Central  Google Scholar 

  11. Li JY, Suo XL, Li NN, Lei D, Peng JX, Yang J, Duan LR, Qin K, Chen CL, Xi J, Jiang Y, Zeng Y, Gong QY, Peng R (2021) Disrupted brain network topology in drug-naive essential tremor patients with and without depression : a resting state functional magnetic resonance imaging study. Clin Neuroradiol 31:981–992

    Article  PubMed  Google Scholar 

  12. Wei L, Zhang J, Long Z, Wu G-R, Hu X, Zhang Y, Wang J (2014) Reduced topological efficiency in cortical-basal Ganglia motor network of Parkinson’s disease: a resting state fMRI study. PLoS One 9:e108124

    Article  PubMed  PubMed Central  Google Scholar 

  13. Suo X, Lei D, Li N, Li W, Kemp GJ, Sweeney JA, Peng R, Gong Q (2021) Disrupted morphological grey matter networks in early-stage Parkinson’s disease. Brain Struct Funct 226:1389–1403

    Article  PubMed  PubMed Central  Google Scholar 

  14. Prajapati R, Emerson IA (2021) Global and regional connectivity analysis of resting-state function MRI brain images using graph theory in Parkinson’s disease. Int J Neurosci 131:105–115

    Article  PubMed  Google Scholar 

  15. Song C, Zhao W, Jiang H, Liu X, Duan Y, Yu X, Yu X, Zhang J, Kui J, Liu C, Tang Y (2021) Stability evaluation of brain changes in Parkinson’s disease based on machine learning. Front Comput Neurosci 15:735991

    Article  PubMed  PubMed Central  Google Scholar 

  16. Li Q, Tao L, Xiao P, Gui H, Xu B, Zhang X, Zhang X, Chen H, Wang H, He W, Lv F, Cheng O, Luo J, Man Y, Xiao Z, Fang W (2022) Combined brain network topological metrics with machine learning algorithms to identify essential tremor. Front Neurosci 16:1035153. https://doi.org/10.3389/fnins.2022.1035153

  17. Xiao P, Tao L, Zhang X, Li Q, Gui H, Xu B, Zhang X, He W, Chen H, Wang H, Lv F, Luo T, Cheng O, Luo J, Man Y, Xiao Z, Fang W (2023) Using histogram analysis of the intrinsic brain activity mapping to identify essential tremor. Front Neurol 14:1165603. https://doi.org/10.3389/fneur.2023.1165603

  18. Dosenbach NUF, Nardos B, Cohen AL, Fair DA, Power JD, Church JA, Nelson SM, Wig GS, Vogel AC, Lessov-Schlaggar CN, Barnes KA, Dubis JW, Feczko E, Coalson RS, Pruett JR, Barch DM, Petersen SE, Schlaggar BL (2010) Prediction of individual brain maturity using fMRI. Science (New York, N.Y.) 329:1358–1361

    Article  CAS  PubMed  Google Scholar 

  19. Wen W, Zhu W, He Y, Kochan NA, Reppermund S, Slavin MJ, Brodaty H, Crawford J, Xia A, Sachdev P (2011) Discrete neuroanatomical networks are associated with specific cognitive abilities in old age. J Neurosci: Off J Soc Neurosci 31:1204–1212

    Article  CAS  Google Scholar 

  20. Zhang Y, Liu S (2018) Analysis of structural brain MRI and multi-parameter classification for Alzheimer’s disease. Biomed Tech (Berl) 63:427–437

    Article  PubMed  Google Scholar 

  21. He Y, Dagher A, Chen Z, Charil A, Zijdenbos A, Worsley K, Evans A (2009) Impaired small-world efficiency in structural cortical networks in multiple sclerosis associated with white matter lesion load. Brain : J Neurol 132:3366–3379

    Article  Google Scholar 

  22. Zhang B, Liu S, Liu X, Chen S, Ke Y, Qi S, Wei X, Ming D (2022) Discriminating subclinical depression from major depression using multi-scale brain functional features: a radiomics analysis. J Affect Disord 297:542–552

    Article  PubMed  Google Scholar 

  23. Strick PL, Dum RP, Fiez JA (2009) Cerebellum and nonmotor function. Annu Rev Neurosci 32:413–434

    Article  CAS  PubMed  Google Scholar 

  24. 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:e69199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Buijink AW, van der Stouwe AM, Broersma M, Sharifi S, Groot PF, Speelman JD, Maurits NM, van Rootselaar AF (2015) Motor network disruption in essential tremor: a functional and effective connectivity study. Brain 138:2934–2947

    Article  PubMed  Google Scholar 

  26. Crowell AL, Ryapolova-Webb ES, Ostrem JL, Galifianakis NB, Shimamoto S, Lim DA, Starr PA (2012) Oscillations in sensorimotor cortex in movement disorders: an electrocorticography study. Brain : J Neurol 135:615–630

    Article  Google Scholar 

  27. Zhu J, Zeng Q, Shi Q, Li J, Dong S, Lai C, Cheng G (2021) Altered brain functional network in subtypes of Parkinson’s disease: a dynamic perspective. Front Aging Neurosci 13:710735

    Article  PubMed  PubMed Central  Google Scholar 

  28. Pang H, Yu Z, Yu H, Cao J, Li Y, Guo M, Cao C, Fan G (2021) Use of machine learning method on automatic classification of motor subtype of Parkinson’s disease based on multilevel indices of rs-fMRI. Parkinsonism Relat Disord 90:65–72

    Article  PubMed  Google Scholar 

  29. Sadler CM, Kami AT, Nantel J, Carlsen AN (2021) Transcranial direct current stimulation of supplementary motor area improves upper limb kinematics in Parkinson’s disease. Clin Neurophysiol: Off J Int Fed Clin Neurophysiol 132:2907–2915

    Article  Google Scholar 

  30. Hamada M, Ugawa Y, Tsuji S (2008) High-frequency rTMS over the supplementary motor area for treatment of Parkinson’s disease. Mov Disord: Off J Mov Disord Soc 23:1524–1531

    Article  Google Scholar 

  31. Shirota Y, Ohtsu H, Hamada M, Enomoto H, Ugawa Y (2013) Supplementary motor area stimulation for Parkinson disease: a randomized controlled study. Neurology 80:1400–1405

    Article  PubMed  Google Scholar 

  32. Wang Y, Sun K, Liu Z, Chen G, Jia Y, Zhong S, Pan J, Huang L, Tian J (2020) Classification of unmedicated bipolar disorder using whole-brain functional activity and connectivity: a radiomics analysis. Cereb Cortex 30:1117–1128

    Article  PubMed  Google Scholar 

  33. Rolls ET (2019) The cingulate cortex and limbic systems for emotion, action, and memory. Brain Struct Funct 224:3001–3018

    Article  PubMed  PubMed Central  Google Scholar 

  34. Maier F, Greuel A, Hoock M, Kaur R, Tahmasian M, Schwartz F, Csoti I, Jessen F, Drzezga A, van Eimeren T, Timmermann L, Eggers C (2023) Impaired self-awareness of cognitive deficits in Parkinson’s disease relates to cingulate cortex dysfunction. Psychol Med 53:1244–1253

    Article  PubMed  Google Scholar 

  35. Prange S, Metereau E, Maillet A, Lhommée E, Klinger H, Pelissier P, Ibarrola D, Heckemann RA, Castrioto A, Tremblay L, Sgambato V, Broussolle E, Krack P, Thobois S (2019) Early limbic microstructural alterations in apathy and depression in de novo Parkinson’s disease. Mov Disord : Off J Mov Disord Soc 34:1644–1654

    Article  Google Scholar 

  36. Wang H, Chen H, Wu J, Tao L, Pang Y, Gu M, Lv F, Luo T, Cheng O, Sheng K, Luo J, Hu Y, Fang W (2018) Altered resting-state voxel-level whole-brain functional connectivity in depressed Parkinson’s disease. Parkinsonism Relat Disord 50:74–80

    Article  PubMed  Google Scholar 

  37. Kelley TA, Serences JT, Giesbrecht B, Yantis S (2008) Cortical mechanisms for shifting and holding visuospatial attention. Cereb Cortex 18:114–125

    Article  PubMed  Google Scholar 

  38. Esterman M, Chiu Y-C, Tamber-Rosenau BJ, Yantis S (2009) Decoding cognitive control in human parietal cortex. Proc Natl Acad Sci USA 106:17974–17979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Boord P, Madhyastha TM, Askren MK, Grabowski TJ (2017) Executive attention networks show altered relationship with default mode network in PD. NeuroImage Clin 13:1–8

    Article  PubMed  Google Scholar 

  40. Kawashima S, Shimizu Y, Ueki Y, Matsukawa N (2021) Impairment of the visuospatial working memory in the patients with Parkinson’s disease: an fMRI study. BMC Neurol 21:335

    Article  PubMed  PubMed Central  Google Scholar 

  41. Madelein van der Stouwe AM, Nieuwhof F, Helmich RC (2020) Tremor pathophysiology: lessons from neuroimaging. Curr Opin Neurol 33:474–481

    Article  CAS  PubMed  Google Scholar 

  42. Hallett M (2012) Parkinson’s disease tremor: pathophysiology. Parkinsonism Relat Disord 18(Suppl 1):S85–S86

    Article  PubMed  Google Scholar 

  43. Luo C, Song W, Chen Q, Yang J, Gong Q, Shang H-F (2017) White matter microstructure damage in tremor-dominant Parkinson’s disease patients. Neuroradiology 59:691–698

    Article  PubMed  Google Scholar 

  44. Lin F, Wu D, Yu J, Weng H, Chen L, Meng F, Chen Y, Ye Q, Cai G (2021) Comparison of efficacy of deep brain stimulation and focused ultrasound in parkinsonian tremor: a systematic review and network meta-analysis. J Neurol Neurosurg Psychiatr 18:jnnp-2020-323656. https://doi.org/10.1136/jnnp-2020-323656

  45. Caparros-Lefebvre D, Ruchoux MM, Blond S, Petit H, Percheron G (1994) Long-term thalamic stimulation in Parkinson’s disease: postmortem anatomoclinical study. Neurology 44:1856–1860

    Article  CAS  PubMed  Google Scholar 

  46. Cury RG, Fraix V, Castrioto A, Pérez Fernández MA, Krack P, Chabardes S, Seigneuret E, Alho EJL, Benabid A-L, Moro E (2017) Thalamic deep brain stimulation for tremor in Parkinson disease, essential tremor, and dystonia. Neurology 89:1416–1423

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank all participants for their participation.

Funding

This research was supported by the National Natural Science Foundation of China (NSFC: 81671663) and the Natural Science Foundation of Chongqing (NSFCQ: cstc2014jcyjA10047).

Author information

Authors and Affiliations

  1. Department of Radiology, The First Affiliated Hospital of Chongqing Medical University, No. 1 Youyi Road, Yuzhong District, Chongqing, 400016, China

    Pan Xiao, Qin Li, Honge Gui, Bintao Xu, Xiaole Zhao, Hongyu Wang, Li Tao, Huiyue Chen, Hansheng Wang, Fajin Lv, Tianyou Luo & Weidong Fang

  2. Department of Neurology, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China

    Oumei Cheng, Jin Luo, Yun Man & Zheng Xiao

Authors
  1. Pan Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qin Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Honge Gui
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bintao Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiaole Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hongyu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Li Tao
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Huiyue Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hansheng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Fajin Lv
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Tianyou Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Oumei Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Jin Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Yun Man
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Zheng Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Weidong Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Pan Xiao and Qin Li: research project—conception and execution; statistical analysis—design and execution; and manuscript preparation—writing of the first draft. Honge Gui and Bintao Xu: research project—execution; statistical analysis—execution, review, and critique; and manuscript preparation—review and critique. Xiaole Zhao and Hongyu Wang: research project—conception and organization; statistical analysis—design and execution; and manuscript preparation—writing of the first draft. Li Tao, Huiyue Chen, and Hansheng Wang: research project—execution; statistical analysis—review and critique; and manuscript preparation—review and critique. Fajin Lv and Tianyou Luo: research project—execution, and manuscript preparation—review and critique. Oumei Cheng, Jing Luo, Yun Man, and Zheng Xiao: research project—execution, and manuscript preparation—review and critique. Weidong Fang: research project—conception and organization; statistical analysis—design, execution, review, and critique; and manuscript preparation—review and critique.

Corresponding author

Correspondence to Weidong Fang.

Ethics declarations

Ethics approval

The studies involving human participants were reviewed and approved by the Ethics Committee of the First Affiliated Hospital of Chongqing Medical University.

Consent to participate

All subjects gave written informed consent in accordance with the Declaration of Helsinki.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 482 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xiao, P., Li, Q., Gui, H. et al. Combined brain topological metrics with machine learning to distinguish essential tremor and tremor-dominant Parkinson’s disease. Neurol Sci (2024). https://doi.org/10.1007/s10072-024-07472-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10072-024-07472-1

Keywords

Search

Navigation