Skip to main content
SpringerLink
Log in

Overlapping stimulation of subthalamic nucleus and dentato-rubro-thalamic tract in Parkinson’s disease after deep brain stimulation

  • Original Article
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Background

Deep brain stimulation (DBS) of the subthalamic nucleus (STN) reduces tremor, rigidity, and akinesia. According to the literature, the dentato-rubro-thalamic tract (DRTt) is verified target for DBS in essential tremor; however, its role in the treatment of Parkinson’s disease is only vaguely described. The aim of our study was to identify the relationship between symptom alleviation in PD patients and the distance of the DBS electrode electric field (EF) to the DRTt.

Methods

A single-center retrospective analysis of patients (N = 30) with idiopathic Parkinson’s disease (PD) who underwent DBS between November 2018 and January 2020 was performed. DRTt and STN were visualized using diffusion-weighted imaging (DWI) and tractography protocol of magnetic resonance (MR). The EF was calculated and compared with STN and course of DRTt. Evaluation of patients before and after surgery was performed with use of UPDRS-III scale. The association between distance from EF to DRTt and clinical outcomes was examined. To confirm the anatomical variation between DRTt and STN observed in tractography, white matter dissection was performed with the Klingler technique on ten human brains.

Results

Patients with EF overlapping STN and DRTt benefited from significant motor symptoms improvement. Anatomical findings confirmed the presence of population differences in variability of the DRTt course and were consistent with the DRTt visualized by MR.

Conclusions

DRTt proximity to STN, the main target in PD DBS surgery, confirmed by DWI with tractography protocol of MR combined with proper predefined stimulation parameters may improve efficacy of DBS-STN.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

Raw data are presented in the manuscript and in the supplementary materials.

Abbreviations

DBS:

Deep brain stimulation

STN:

Subthalamic nucleus

DRTt:

Dentato-rubro-thalamic tract

PD:

Parkinson’s disease

EF:

Electric field

MR:

Magnetic resonance

DWI:

Diffusion-weighted imaging

FCT:

Fasciculus cerebellothalamicus

RN:

Red nucleus

ROI:

Region of interest

DN:

Dentate nucleus

MCP:

Middle cerebellar peduncle

SCP:

Superior cerebellar peduncle

VTA:

Volume tissue activated

References

  1. Abdulbaki A, Kaufmann J, Galazky I, Buentjen L, Voges J (2021) Neuromodulation of the subthalamic nucleus in Parkinson’s disease: the effect of fiber tract stimulation on tremor control. Acta Neurochir (Wien). 163(1):185–195. https://doi.org/10.1007/s00701-020-04495-3

    Article  PubMed  Google Scholar 

  2. Afifi AK, Bergman RA (2005) Functional neuroanatomy: text and atlas, 2nd edn. Lange Medical Books/McGraw-Hill, New York

    Google Scholar 

  3. Agrawal A, Kapfhammer JP, Kress A, Wichers H, Deep A, Feindel W et al (2011) Josef Klingler’s models of white matter tracts: influences on neuroanatomy, neurosurgery, and neuroimaging. Neurosurgery. 69(2):238–52. https://doi.org/10.1227/NEU.0b013e318214ab79. (discussion 252-4)

    Article  PubMed  Google Scholar 

  4. Le Bihan D, Poupon C, Amadon A, Lethimonnier F (2006) Artifacts and pitfalls in diffusion MRI. J Magn Reson Imaging 24(3):478–488. https://doi.org/10.1002/jmri.20683

    Article  PubMed  Google Scholar 

  5. Cavallieri F, Fraix V, Bove F, Mulas D, Tondelli M, Castrioto A et al (2021) Predictors of long-term outcome of subthalamic stimulation in Parkinson disease. Ann Neurol 89(3):587–597. https://doi.org/10.1002/ana.25994

    Article  PubMed  CAS  Google Scholar 

  6. Coenen VA, Allert N, Mädler B (2011) A role of diffusion tensor imaging fiber tracking in deep brain stimulation surgery: DBS of the dentato-rubro-thalamic tract (drt) for the treatment of therapy-refractory tremor. Acta Neurochir (Wien). 153(8):1579–85. https://doi.org/10.1007/s00701-011-1036-z. (discussion 1585)

    Article  PubMed  Google Scholar 

  7. Coenen VA, Allert N, Mädler B (2011) A role of diffusion tensor imaging fiber tracking in deep brain stimulation surgery: DBS of the dentato-rubro-thalamic tract (drt) for the treatment of therapy-refractory tremor. Acta Neurochir (Wien). 153(8):1579–85 (discussion 1585)

    Article  PubMed  Google Scholar 

  8. Coenen VA, Allert N, Paus S, Kronenbürger M, Urbach H, Mädler B (2014) Modulation of the cerebello-thalamo-cortical network in thalamic deep brain stimulation for tremor: a diffusion tensor imaging study. Neurosurgery. 75(6):657–69 (discussion 669-70)

    Article  PubMed  Google Scholar 

  9. Coenen VA, Allert N, Paus S, Kronenbürger M, Urbach H, Mädler B (2014) Modulation of the cerebello-thalamo-cortical network in thalamic deep brain stimulation for tremor: a diffusion tensor imaging study. Neurosurgery. 75(6):657–69. https://doi.org/10.1227/NEU.0000000000000540. (discussion 669-70)

    Article  PubMed  Google Scholar 

  10. Coenen VA, Madler B, Schiffbauer H, Urbach H, Allert N (2011) Individual fiber anatomy of the subthalamic region revealed with diffusion tensor imaging: a concept to identify the deep brain stimulation target for tremor suppression. Neurosurgery. 68(4):1069–75. https://doi.org/10.1227/NEU.0b013e31820a1a20. (discussion 1075–6)

    Article  PubMed  Google Scholar 

  11. Deuter D, Torka E, Kohl Z, Schmidt NO, Schlaier J (2023) Mediation of tremor control by the decussating and nondecussating part of the dentato-rubro-thalamic tract in deep brain stimulation in essential tremor: which part should be stimulated? Neuromodulation 26(8):1668–1679. https://doi.org/10.1016/j.neurom.2022.04.040

    Article  PubMed  Google Scholar 

  12. Fenoy AJ, Schiess MC (2017) Deep brain stimulation of the dentato-rubro-thalamic tract: outcomes of direct targeting for tremor. Neuromodulation 20(5):429–436. https://doi.org/10.1111/ner.12585

    Article  PubMed  Google Scholar 

  13. Follett KA, Weaver FM, Stern M, Hur K, Harris CL, Luo P et al (2010) Pallidal versus subthalamic deep-brain stimulation for Parkinson’s disease. N Engl J Med. 362(22):2077–91

    Article  PubMed  CAS  Google Scholar 

  14. Gallay MN, Jeanmonod D, Liu J, Morel A (2008) Human pallidothalamic and cerebellothalamic tracts: anatomical basis for functional stereotactic neurosurgery. Brain Struct Funct 212(6):443–463. https://doi.org/10.1007/s00429-007-0170-0

    Article  PubMed  PubMed Central  Google Scholar 

  15. Gaytán-Tocavén L, Olvera-Cortés ME (2004) Bilateral lesion of the cerebellar-dentate nucleus impairs egocentric sequential learning but not egocentric navigation in the rat. Neurobiol Learn Mem 82(2):120–127. https://doi.org/10.1016/j.nlm.2004.05.006

    Article  PubMed  Google Scholar 

  16. Güngör A, Baydın ŞS, Holanda VM, Middlebrooks EH, Isler C, Tugcu B et al (2018) Microsurgical anatomy of the subthalamic nucleus: correlating fiber dissection results with 3-T magnetic resonance imaging using neuronavigation. J Neurosurg 130(3):716–732. https://doi.org/10.3171/2017.10.JNS171513

    Article  PubMed  Google Scholar 

  17. JD Carrillo-Ruiz (2012) Topics in neuromodulation treatment. Chapter 4 IntechOpen

  18. Krack P, Batir A, Van Blercom N, Chabardes S, Fraix V, Ardouin C et al (2003) Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med. 349(20):1925–34

    Article  PubMed  CAS  Google Scholar 

  19. Kwon HG, Hong JH, Hong CP, Lee DH, Ahn SH, Jang SH (2011) Dentatorubrothalamic tract in human brain: diffusion tensor tractography study. Neuroradiology 53(10):787–791. https://doi.org/10.1007/s00234-011-0878-7

    Article  PubMed  Google Scholar 

  20. Limousin P, Krack P, Pollak P, Benazzouz A, Ardouin C, Hoffmann D et al (1998) Electrical stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med. 339(16):1105–11

    Article  PubMed  CAS  Google Scholar 

  21. Lozano AM (2000) Vim thalamic stimulation for tremor. Arch Med Res. 31(3):266–9

    Article  PubMed  CAS  Google Scholar 

  22. Mandrekar JN (2010) Receiver operating characteristic curve in diagnostic test assessment. J Thorac Oncol 5(9):1315–1316

    Article  PubMed  Google Scholar 

  23. Mendoza JE, Foundas AL (2007) Clinical neuroanatomy: a neurobehavioral approach. Springer, New York

    Google Scholar 

  24. Meola A, Comert A, Yeh FC, Sivakanthan S, Fernandez-Miranda JC (2016) The nondecussating pathway of the dentatorubrothalamic tract in humans: human connectome-based tractographic study and microdissection validation. J Neurosurg 124(5):1406–1412. https://doi.org/10.3171/2015.4.JNS142741

    Article  PubMed  Google Scholar 

  25. Middlebrooks EH, Domingo RA, Vivas-Buitrago T, Okromelidze L, Tsuboi T, Wong JK et al (2020) Neuroimaging advances in deep brain stimulation: review of indications, Anatomy, and Brain Connectomics. AJNR Am J Neuroradiol 41(9):1558–1568. https://doi.org/10.3174/ajnr.A6693

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Middleton FA, Strick PL (1998) Cerebellar output: motor and cognitive channels. Trends Cogn Sci 2(9):348–354. https://doi.org/10.1016/s1364-6613(98)01220-0

    Article  PubMed  CAS  Google Scholar 

  27. Mori S, Crain BJ, Chacko VP, van Zijl PC (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45(2):265–269. https://doi.org/10.1002/1531-8249(199902)45:2%3c265::aid-ana21%3e3.0.co;2-3

    Article  PubMed  CAS  Google Scholar 

  28. Muller J, Alizadeh M, Mohamed FB, Riley J, Pearce JJ, Trieu B, Liang T, Romo V, Sharan A, Wu C (2019) Clinically applicable delineation of the pallidal sensorimotor region in patients with advanced Parkinson’s disease: study of probabilistic and deterministic tractography. J Neurosurg JNS 131(5):1520–1531. https://doi.org/10.3171/2018.7.JNS18541

    Article  Google Scholar 

  29. Naidich TP, Duvernoy HM, Delman BN, Sorensen AG, Kollias SS, Haacke EM (2009) Duvernoy’s atlas of the human brain stem and cerebellum. Springer Vienna. https://doi.org/10.1007/978-3-211-73971-6

  30. Obeso JA, Olanow CW, Rodriguez-Oroz MC, Krack P, Kumar R, Lang AE (2001) Deep-brain stimulation of the subthalamic nucleus or the pars interna of the globus pallidus in Parkinson’s disease. N Engl J Med. 345(13):956–63

    Article  PubMed  CAS  Google Scholar 

  31. Oertel MF, Schüpbach WM, Ghika JA, Stieglitz LH, Fiechter M, Kaelin-Lang A et al (2017) Combined thalamic and subthalamic deep brain stimulation for tremor-dominant Parkinson’s disease. Acta Neurochir (Wien) 159(2):265–269

    Article  PubMed  Google Scholar 

  32. Perlmutter JS, Mink JW (2006) Deep brain stimulation. Annu Rev Neurosci 29:229–257

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Petersen KJ, Reid JA, Chakravorti S, Juttukonda MR, Franco G, Trujillo P et al (2018) Structural and functional connectivity of the nondecussating dentato-rubro-thalamic tract. Neuroimage 1(176):364–371. https://doi.org/10.1016/j.neuroimage.2018.04.074

    Article  Google Scholar 

  34. Postuma RB, Berg D, Stern M, Poewe W, Olanow CW, Oertel W et al (2015) MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord 30(12):1591–1601. https://doi.org/10.1002/mds.26424

    Article  PubMed  Google Scholar 

  35. Prent N, Potters WV, Boon LI, Caan MWA, de Bie RMA, van den Munckhof P, Schuurman PR, van Rootselaar A (2020) Distance to white matter tracts is associated with deep brain stimulation motor outcome in Parkinson’s disease. J Neurosurg JNS 133(2):433–442. https://doi.org/10.3171/2019.5.JNS1952

    Article  Google Scholar 

  36. Rodriguez-Oroz MC, Obeso JA, Lang AE, Houeto JL, Pollak P, Rehncrona S et al (2005) Bilateral deep brain stimulation in Parkinson’s disease: a multicentre study with 4 years follow-up. Brain 128(Pt 10):2240–2249

    Article  PubMed  CAS  Google Scholar 

  37. Sarwar T, Ramamohanarao K, Zalesky A (2019) Mapping connectomes with diffusion MRI: deterministic or probabilistic tractography? Magn Reson Med 81(2):1368–1384. https://doi.org/10.1002/mrm.27471

    Article  PubMed  Google Scholar 

  38. Schlaier J, Anthofer J, Steib K, Fellner C, Rothenfusser E, Brawanski A et al (2015) Deep brain stimulation for essential tremor: targeting the dentato-rubro-thalamic tract? Neuromodulation 18(2):105–112

    Article  PubMed  Google Scholar 

  39. Schuepbach WM, Rau J, Knudsen K, Volkmann J, EARLYSTIM Study Group (2013) Neurostimulation for Parkinson’s disease with early motor complications. N Engl J Med. 368(7):610–22. https://doi.org/10.1056/NEJMoa1205158

    Article  PubMed  CAS  Google Scholar 

  40. Silva SM, Cunha-Cabral D, Andrade JP (2017) Neurosurgical relevance of the dissection of the diencephalic white matter tracts using the Klingler technique. Clin Neurol Neurosurg 156:35–40. https://doi.org/10.1016/j.clineuro.2017.03.001

    Article  PubMed  Google Scholar 

  41. Sweet JA, Walter BL, Gunalan K, Chaturvedi A, McIntyre CC, Miller JP (2014) Fiber tractography of the axonal pathways linking the basal ganglia and cerebellum in Parkinson disease: implications for targeting in deep brain stimulation. J Neurosurg 120(4):988–996. https://doi.org/10.3171/2013.12.JNS131537

    Article  PubMed  PubMed Central  Google Scholar 

  42. Tabbal SD, Revilla FJ, Mink JW, Schneider-Gibson P, Wernle AR, de Erausquin GA et al (2007) Safety and efficacy of subthalamic nucleus deep brain stimulation performed with limited intraoperative mapping for treatment of Parkinson’s disease. Neurosurgery. 61(3 Suppl):119–27. https://doi.org/10.1227/01.neu.0000289725.97211.51. (discussion 127-9)

    Article  PubMed  Google Scholar 

  43. Tacyildiz AE, Bilgin B, Gungor A, Ucer M, Karadag A, Tanriover N (2021) Dentate nucleus: connectivity-based anatomic parcellation based on superior cerebellar peduncle projections. World Neurosurg 152:e408–e428. https://doi.org/10.1016/j.wneu.2021.05.102

    Article  PubMed  Google Scholar 

  44. Tsai ST, Lin SH, Chou YC, Pan YH, Hung HY, Li CW, Lin SZ, Chen SY (2009) Prognostic factors of subthalamic stimulation in Parkinson’s disease: a comparative study between short- and long-term effects. Stereotact Funct Neurosurg 87(4):241–248. https://doi.org/10.1159/000225977

    Article  PubMed  Google Scholar 

  45. Wathen CA, Frizon LA, Maiti TK, Baker KB, Machado AG (2018) Deep brain stimulation of the cerebellum for poststroke motor rehabilitation: from laboratory to clinical trial. Neurosurg Focus 45(2):E13. https://doi.org/10.3171/2018.5.FOCUS18164

    Article  PubMed  Google Scholar 

  46. Williams A, Gill S, Varma T, Jenkinson C, Quinn N, Mitchell R et al (2010) Deep brain stimulation plus best medical therapy versus best medical therapy alone for advanced Parkinson’s disease (PD SURG trial): a randomised, open-label trial. Lancet Neurol 9(6):581–591. https://doi.org/10.1016/S1474-4422(10)70093-4

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neurosurgery and Neurooncology, Medical University of Łódź, Barlicki University Hospital, Łódź, Poland

    K. Wiśniewski, K. Zaczkowski, A. Szulia, R. Wójcik, E. J. Bobeff, K. Kwiecień & D. J. Jaskólski

  2. Department of Extrapyramidal Diseases, Medical University of Łódź, Łódź, Poland

    A. Gajos & A. Bogucki

  3. Department of Descriptive and Clinical Anatomy, Medical University of Warsaw, Warsaw, Poland

    M. Grzegorczyk & B. Ciszek

  4. Department of Forensic Medicine, Medical University of Warsaw, Warsaw, Poland

    A. Dąbkowska

  5. Department of Neurosurgery, University of California, San Diego, San Diego, CA, 92123, USA

    M. G. Brandel

  6. Department of Medical Sciences, Section of Neurosurgery, Uppsala University, Uppsala, Sweden

    A. Fahlström

  7. Department of Sleep Medicine and Metabolic Disorders, Medical University of Lodz, Łódź, Poland

    E. J. Bobeff

Authors
  1. K. Wiśniewski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Gajos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K. Zaczkowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Szulia
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Grzegorczyk
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. Dąbkowska
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. R. Wójcik
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. E. J. Bobeff
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. K. Kwiecień
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. M. G. Brandel
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. A. Fahlström
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. A. Bogucki
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. B. Ciszek
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. D. J. Jaskólski
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization—Karol Wiśniewski. Methodology—Karol Wiśniewski, Agata Gajos, Andreas Fahlström. Analysis—Karol Wiśniewski, Agata Gajos, Andrzej Bogucki, Michał Grzegorczyk, Michael G. Brandel. Investigation—Karol Wiśniewski, Karol Zaczkowski, Agata Szulia, Michał Grzegorczyk, Agnieszka Dąbkowska, Andreas Fahlström, Ernest J. Bobeff, Rafał Wójcik, Katarzyna Kwiecień. Writing—original draft preparation—Karol Wiśniewski, Karol Zaczkowski, Agata Szulia, Agata Gajos, Andreas Fahlström, Ernest Jan Bobeff, Michael G. Brandel. Writing—review and editing—Karol Wiśniewski, Agata Gajos, Andrzej Bogucki, Bogdan Ciszek, Dariusz J. Jaskólski. Project administration—Karol Wiśniewski. Supervision—Karol Wiśniewski, Agata Gajos, Andrzej Bogucki, Bogdan Ciszek, Dariusz J. Jaskólski. All authors reviewed the manuscript.

Corresponding author

Correspondence to K. Wiśniewski.

Ethics declarations

Ethical approval

The study protocol was approved by the Bioethics Committee of the Medical University of Lodz (no. RNN/205/22KE).

Consent to participate

This article does not contain any studies involving human participants or animals performed by any of the authors; thus, no formal consent is required for this type of study.

Consent for publication

All authors approved the article.

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.

Comments

The authors of this paper did a Herculean job trying to find an explanation for different effects of STN DBS on tremor control in Parkinson disease patients—by correlating the stimulated regions with the course of the dentate-rubro-thalamic tract. In addition to deep radiographic analysis of their own clinical cohort, the authors performed a thorough literature search and completed a sophisticated anatomical study, confirming the variability of the tract's location and the distance between the tract and STN.

Despite inherent subjectivity of the tractographic imaging and unclear reliability of the fiber dissection in brains of unaffected subjects, one has to wonder if the authors' findings explain tremendous variability in degree of individual response to rather standard and decades-old neurosurgical procedure where stimulation of clearly identifiable target may or may not require additional refinement based on the patient's response. Such variability once again underscores the value of physiological (rather than solely radiographic or anatomical) targeting—at least until more reliable indicators for proper targeting are established.

I applaud the authors for the thoroughness of their investigation and look forward to seeing more data to support their findings and postulates.

Konstantin Slavin,

Chicago, USA

Supplementary information 

ESM 1

DOCX (21.9 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

Wiśniewski, K., Gajos, A., Zaczkowski, K. et al. Overlapping stimulation of subthalamic nucleus and dentato-rubro-thalamic tract in Parkinson’s disease after deep brain stimulation. Acta Neurochir 166, 106 (2024). https://doi.org/10.1007/s00701-024-06006-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00701-024-06006-0

Keywords

Search

Navigation