Use of probabilistic tractography to provide reliable distinction of the motor and sensory thalamus for prospective targeting during asleep deep brain stimulation

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  • 1 Department of Neurological Surgery, Vickie and Jack Farber Institute for Neuroscience, Thomas Jefferson University, Philadelphia, Pennsylvania;
  • | 2 Jefferson Integrated Magnetic Resonance Imaging Center, Department of Radiology, Thomas Jefferson University, Philadelphia, Pennsylvania;
  • | 3 Department of Anesthesia, Thomas Jefferson University, Philadelphia, Pennsylvania;
  • | 4 Department of Neurology, Christiana Care Health System, Newark, Delaware; and
  • | 5 Department of Neurology, Thomas Jefferson University, Philadelphia, Pennsylvania
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OBJECTIVE

Accurate electrode placement is key to effective deep brain stimulation (DBS). The ventral intermediate nucleus (VIM) of the thalamus is an established surgical target for the treatment of essential tremor (ET). Retrospective tractography-based analysis of electrode placement has associated successful outcomes with modulation of motor input to VIM, but no study has yet evaluated the feasibility and efficacy of prospective presurgical tractography-based targeting alone. Therefore, the authors sought to demonstrate the safety and efficacy of probabilistic tractography–based VIM targeting in ET patients and to perform a systematic comparison of probabilistic and deterministic tractography.

METHODS

Fourteen patients with ET underwent preoperative diffusion imaging. Probabilistic tractography was applied for preoperative targeting, and deterministic tractography was performed as a comparison between methods. Tractography was performed using the motor and sensory areas as initiation seeds, the ipsilateral thalamus as an inclusion mask, and the contralateral dentate nucleus as a termination mask. Tract-density maps consisted of voxels with 10% or less of the maximum intensity and were superimposed onto anatomical images for presurgical planning. Target planning was based on probabilistic tract-density images and indirect target coordinates. Patients underwent robotic image-guided, image-verified implantation of directional DBS systems. Postoperative tremor scores with and without DBS were recorded. The center of gravity and Dice similarity coefficients were calculated and compared between tracking methods.

RESULTS

Prospective probabilistic targeting of VIM was successful in all 14 patients. All patients experienced significant tremor reduction. Formal postoperative tremor scores were available for 9 patients, who demonstrated a mean 68.0% tremor reduction. Large differences between tracking methods were observed across patients. Probabilistic tractography–identified VIM fibers were more anterior, lateral, and superior than deterministic tractography–identified fibers, whereas probabilistic tractography–identified ventralis caudalis fibers were more posterior, lateral, and superior than deterministic tractography–identified fibers. Deterministic methods were unable to clearly distinguish between motor and sensory fibers in the majority of patients, but probabilistic methods produced distinct separation.

CONCLUSIONS

Probabilistic tractography–based VIM targeting is safe and effective for the treatment of ET. Probabilistic tractography is more precise than deterministic tractography for the delineation of VIM and the ventralis caudalis nucleus of the thalamus. Deterministic algorithms tended to underestimate separation between motor and sensory fibers, which may have been due to its limitations with crossing fibers. Larger studies across multiple centers are necessary to further validate this method.

ABBREVIATIONS

CoG = center of gravity; DBS = deep brain stimulation; DSC = Dice similarity coefficient; DWI = diffusion-weighted imaging; ET = essential tremor; GPU = graphics processing unit; PM = probability map; TDI = tract-density image; TETRAS = The Essential Tremor Rating Assessment Scale; VC = ventralis caudalis nucleus; VIM = ventral intermediate nucleus.

Illustration from Serrato-Avila (pp 1410–1423). Copyright Johns Hopkins University, Art as Applied to Medicine. Published with permission.

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  • 1

    Meng FG, Zhang JG, Kao CC, Klein JC, Hilker R. The tremor network targeted by successful VIM deep brain stimulation in humans. Neurology. 2012;79(9):953.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Schlaier JR, Beer AL, Faltermeier R, Fellner C, Steib K, et al. Probabilistic vs. deterministic fiber tracking and the influence of different seed regions to delineate cerebellar-thalamic fibers in deep brain stimulation. Eur J Neurosci. 2017;45(12):16231633.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Al-Fatly B, Ewert S, Kübler D, Kroneberg D, Horn A, Kühn AA. Connectivity profile of thalamic deep brain stimulation to effectively treat essential tremor. Brain. 2019;142(10):30863098.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Gravbrot N, Saranathan M, Pouratian N, Kasoff WS. Advanced imaging and direct targeting of the motor thalamus and dentato-rubro-thalamic tract for tremor: a systematic review. Stereotact Funct Neurosurg. 2020;98(4):220240.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Akram H, Dayal V, Mahlknecht P, Georgiev D, Hyam J, et al. Connectivity derived thalamic segmentation in deep brain stimulation for tremor. Neuroimage Clin. 2018;18(18):130142.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Deistung A, Schäfer A, Schweser F, Biedermann U, Turner R, Reichenbach JR. Toward in vivo histology: a comparison of quantitative susceptibility mapping (QSM) with magnitude-, phase-, and R2*-imaging at ultra-high magnetic field strength. Neuroimage. 2013;65(299):314.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7

    Burchiel KJ, McCartney S, Lee A, Raslan AM. Accuracy of deep brain stimulation electrode placement using intraoperative computed tomography without microelectrode recording. J Neurosurg. 2013;119(2):301306.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Chen T, Mirzadeh Z, Chapple KM, Lambert M, Evidente VGH, et al. Intraoperative test stimulation versus stereotactic accuracy as a surgical end point: a comparison of essential tremor outcomes after ventral intermediate nucleus deep brain stimulation. J Neurosurg. 2018;129(2):290298.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Behrens TEJ, Johansen-Berg H, Woolrich MW, Smith SM, Wheeler-Kingshott CA, et al. Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci. 2003;6(7):750757.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Jakab A, Werner B, Piccirelli M, Kovács K, Martin E, et al. Feasibility of diffusion tractography for the reconstruction of intra-thalamic and cerebello-thalamic targets for functional neurosurgery: a multi-vendor pilot study in four subjects. Front Neuroanat. 2016;10 76.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Jakab A, Blanc R, Berényi EL, Székely G. Generation of individualized thalamus target maps by using statistical shape models and thalamocortical tractography. AJNR Am J Neuroradiol. 2012;33(11):21102116.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Johansen-Berg H, Behrens TEJ, Sillery E, Ciccarelli O, Thompson AJ, et al. Functional-anatomical validation and individual variation of diffusion tractography-based segmentation of the human thalamus. Cereb Cortex. 2005;15(1):3139.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Pouratian N, Zheng Z, Bari AA, Behnke E, Elias WJ, Desalles AAF. Multi-institutional evaluation of deep brain stimulation targeting using probabilistic connectivity-based thalamic segmentation. J Neurosurg. 2011;115(5):9951004.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Sammartino F, Krishna V, King NKK, Lozano AM, Schwartz ML, et al. Tractography-based ventral intermediate nucleus targeting: novel methodology and intraoperative validation. Mov Disord. 2016;31(8):12171225.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Lozano AM. Vim thalamic stimulation for tremor. Arch Med Res. 2000;31(3):266269.

  • 16

    Petersen MV, Lund TE, Sunde N, Frandsen J, Rosendal F, et al. Probabilistic versus deterministic tractography for delineation of the cortico-subthalamic hyperdirect pathway in patients with Parkinson disease selected for deep brain stimulation. J Neurosurg. 2017;126(5):16571668.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Behrens TEJ, Woolrich MW, Jenkinson M, et al. Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med. 2003;50(5):10771088.

  • 18

    Jeurissen B, Leemans A, Tournier JD, Jones DK, Sijbers J. Investigating the prevalence of complex fiber configurations in white matter tissue with diffusion magnetic resonance imaging. Hum Brain Mapp.2013;34(11):27472766.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Descoteaux M, Deriche R, Knösche TR, Anwander A. Deterministic and probabilistic tractography based on complex fibre orientation distributions. IEEE Trans Med Imaging. 2009;28(2):269286.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Ondo WG, Pascual B. Tremor Research Group Essential Tremor Rating Scale (TETRAS): Assessing impact of different item instructions and procedures. Tremor Other Hyperkinet Mov (N Y).2020;10(1):36.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21

    Muller J, Alizadeh M, Mohamed FB, Riley J, Pearce JJ, et al. Clinically applicable delineation of the pallidal sensorimotor region in patients with advanced Parkinson’s disease: study of probabilistic and deterministic tractography. J Neurosurg. 2019;131(5):15201531.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22

    D’Haese PF, Pallavaram S, Li R, Remple MS, Kao C, et al. CranialVault and its CRAVE tools: a clinical computer assistance system for deep brain stimulation (DBS) therapy. Med Image Anal. 2012;16(3):744753.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis: I. Segmentation and surface reconstruction. NeuroImage. 1999;9(2):179194.

  • 24

    Caulo M, Briganti C, Mattei PA, Perfetti B, Ferretti A, et al. New morphologic variants of the hand motor cortex as seen with MR imaging in a large study population. AJNR Am J Neuroradiol. 2007;28(8):14801485.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25

    Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, et al. User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage. 2006;31(3):11161128.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Mohammadi S, Möller HE, Kugel H, Müller DK, Deppe M. Correcting eddy current and motion effects by affine whole-brain registrations: evaluation of three-dimensional distortions and comparison with slicewise correction. Magn Reson Med. 2010;64(4):10471056.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Behrens TEJ, Woolrich MW, Jenkinson M, Johansen-Berg H, Nunes RG, et al. Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med. 2003;50(5):10771088.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Kincses ZT, Szabó N, Valálik I, Kopniczky Z, Dézsi L, et al. Target identification for stereotactic thalamotomy using diffusion tractography. PLoS One. 2012;7(1):e29969.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Osenbach R, Richard K, Burchiel K. Thalamotomy: indications, techniques, and results. In: Germano IM, ed. Neurosurgical Treatment of Movement Disorders.AANS;1998.

    • Search Google Scholar
    • Export Citation
  • 30

    Ponce FA, Lambert M. 207 Direct targeting of the ventral intermediate nucleus using high-field proton density MR imaging: functional outcomes and comparison to “indirect” targeting. Neurosurgery. 2019;66(Supplement 1):65.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31

    Chen T, Mirzadeh Z, Chapple K, Lambert M, Dhall R, Ponce FA. “Asleep” deep brain stimulation for essential tremor. J Neurosurg. 2016;124(6):18421849.

  • 32

    Waugh JL, Kuster JK, Makhlouf ML, et al. A registration method for improving quantitative assessment in probabilistic diffusion tractography. NeuroImage. 2019:288-306.

    • Search Google Scholar
    • Export Citation
  • 33

    Zou KH, Warfield SK, Bharatha A, Tempany CM, Kaus MR, et al. Statistical validation of image segmentation quality based on a spatial overlap index. Acad Radiol. 2004;11(2):178189.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Abosch A, Yacoub E, Ugurbil K, Harel N. An assessment of current brain targets for deep brain stimulation surgery with susceptibility-weighted imaging at 7 tesla. Neurosurgery. 2010;67(6):17451756.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Hirai T, Jones EG. A new parcellation of the human thalamus on the basis of histochemical staining. Brain Res Brain Res Rev. 1989;14(1):134.

  • 36

    Jones EG. The Thalamus. Springer;2012.

  • 37

    Dembek TA, Petry-Schmelzer JN, Reker P, Wirths J, Hamacher S, et al. PSA and VIM DBS efficiency in essential tremor depends on distance to the dentatorubrothalamic tract. Neuroimage Clin. 2020;26(March):102235.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38

    Morrison MA, Lee AT, Martin AJ, Dietiker C, Brown EG, Wang DD. DBS targeting for essential tremor using intersectional dentato-rubro-thalamic tractography and direct proton density visualization of the VIM: technical note on 2 cases. J Neurosurg. 2021;135(3):806814.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39

    Krishna V, Sammartino F, Agrawal P, Changizi BK, Bourekas E, et al. Prospective tractography-based targeting for improved safety of focused ultrasound thalamotomy. Neurosurgery. 2019;84(1):160168.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Akram H, Sotiropoulos SN, Jbabdi S, Georgiev D, Mahlknecht P, et al. Subthalamic deep brain stimulation sweet spots and hyperdirect cortical connectivity in Parkinson’s disease. Neuroimage. 2017;158(332):345.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 41

    Behrens TEJ, Berg HJ, Jbabdi S, Rushworth MFS, Woolrich MW. Probabilistic diffusion tractography with multiple fibre orientations: What can we gain?. Neuroimage. 2007;34(1):144155.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

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