Abstract
Purpose
Deep brain stimulation is a common treatment for medication-refractory essential tremor. Current coordinate-based targeting methods result in variable outcomes due to variation in thalamic structure and the optimal patient-specific functional location. The purpose of this study was to compare the coordinate-based pre-operative targets to patient-specific thalamic segmentation utilizing a probabilistic tractography methodology.
Methods
Using available diffusion MRI of 32 subjects from the Human Connectome Project database, probabilistic tractography was performed. Each thalamic voxel was coded based on one of six predefined cortical targets. The segmentation results were analyzed and compared to a 2-mm spherical target centered at the coordinate-based location of the ventral intermediate thalamic nucleus.
Results
The traditional coordinate-based target had maximal overlap with the junction of the region most connected to primary motor cortex (M1) (36.6 ± 25.7% of voxels on left; 58.1 ± 28.5% on right) and the area connected to the supplementary motor area/premotor cortex (SMA/PMC) (44.9 ± 21.7% of voxels on left; 28.9 ± 22.2% on right). There was a within-subject coefficient of variation from right-to-left of 69.4 and 63.1% in the volume of overlap with the SMA/PMC and M1 regions, respectively.
Conclusion
Thalamic segmentation based on structural connectivity measures is a promising technique that may enhance traditional targeting methods by generating reproducible, patient-specific pre-operative functional targets. Our results highlight the problematic intra- and inter-subject variability of indirect, coordinate-based targets. Future prospective clinical studies will be needed to validate this targeting methodology in essential tremor patients.
Similar content being viewed by others
Abbreviations
- ET:
-
Essential tremor
- DBS:
-
Deep brain stimulator
- Vim:
-
Ventral intermediate nucleus
- Vo:
-
Ventralis oralis
- PMC:
-
Premotor cortex
- SMA:
-
Supplementary motor area
- PFC:
-
Prefrontal cortex
References
Louis ED, Ottman R (2014) How many people in the USA have essential tremor? Deriving a population estimate based on epidemiological data. Tremor Other Hyperkinet Mov (N Y) 4:259
Dogu O, Sevim S, Camdeviren H, Sasmaz T, Bugdayci R, Aral M, Kaleagasi H, Un S, Louis ED (2003) Prevalence of essential tremor: door-to-door neurologic exams in Mersin Province, Turkey. Neurology 61(12):1804–1806. https://doi.org/10.1212/01.WNL.0000099075.19951.8C
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
Louis ED (2001) Clinical practice. Essential tremor. N Engl J Med 345(12):887–891. https://doi.org/10.1056/NEJMcp010928
Benabid AL, Pollak P, Gao D, Hoffmann D, Limousin P, Gay E, Payen I, Benazzouz A (1996) Chronic electrical stimulation of the ventralis intermedius nucleus of the thalamus as a treatment of movement disorders. J Neurosurg 84(2):203–214. https://doi.org/10.3171/jns.1996.84.2.0203
Higuchi MA, Topiol DD, Ahmed B, Morita H, Carbunaru S, Hess CW et al (2015) Impact of an interdisciplinary deep brain stimulation screening model on post-surgical complications in essential tremor patients. PLoS One 10(12):e0145623. https://doi.org/10.1371/journal.pone.0145623
Zhang K, Bhatia S, MY O, Cohen D, Angle C, Whiting D (2010) Long-term results of thalamic deep brain stimulation for essential tremor. J Neurosurg 112(6):1271–1276. https://doi.org/10.3171/2009.10.JNS09371
Foote KD, Okun MS (2005) Ventralis intermedius plus ventralis oralis anterior and posterior deep brain stimulation for posttraumatic Holmes tremor: two leads may be better than one: technical note. Neurosurgery 56(2 Suppl):E445; discussion E
Mehanna R, Machado AG, Oravivattanakul S, Genc G, Cooper SE (2014) Comparing two deep brain stimulation leads to one in refractory tremor. Cerebellum 13(4):425–432. https://doi.org/10.1007/s12311-014-0552-9
Foote KD, Seignourel P, Fernandez HH, Romrell J, Whidden E, Jacobson C, et al (2006) Dual electrode thalamic deep brain stimulation for the treatment of posttraumatic and multiple sclerosis tremor. Neurosurgery 58(4 Suppl 2):ONS-280-285; discussion ONS-285-286
Plaha P, Khan S, Gill SS (2008) Bilateral stimulation of the caudal zona incerta nucleus for tremor control. J Neurol Neurosurg Psychiatry 79(5):504–513. https://doi.org/10.1136/jnnp.2006.112334
Kilbane C, Ramirez-Zamora A, Ryapolova-Webb E, Qasim S, Glass GA, Starr PA, Ostrem JL (2015) Pallidal stimulation for Holmes tremor: clinical outcomes and single-unit recordings in 4 cases. J Neurosurg 122(6):1306–1314. https://doi.org/10.3171/2015.2.JNS141098
Velasco F, Jimenez F, Perez ML, Carrillo-Ruiz JD, Velasco AL, Ceballos J et al (2001) Electrical stimulation of the prelemniscal radiation in the treatment of Parkinson’s disease: an old target revised with new techniques. Neurosurgery 49(2):293–306 discussion 308
Abosch A, Yacoub E, Ugurbil K, Harel N (2010) An assessment of current brain targets for deep brain stimulation surgery with susceptibility-weighted imaging at 7 tesla. Neurosurgery 67(6):1745–1756; discussion 1756. https://doi.org/10.1227/NEU.0b013e3181f74105
Sudhyadhom A, Haq IU, Foote KD, Okun MS, Bova FJ (2009) A high resolution and high contrast MRI for differentiation of subcortical structures for DBS targeting: the fast gray matter acquisition T1 inversion recovery (FGATIR). NeuroImage 47(Suppl 2):T44–T52. https://doi.org/10.1016/j.neuroimage.2009.04.018
King NK, Krishna V, Basha D, Elias G, Sammartino F, Hodaie M et al (2017) Microelectrode recording findings within the tractography-defined ventral intermediate nucleus. J Neurosurg 126(5):1669–1675. https://doi.org/10.3171/2016.3.JNS151992
Kelly PJ, Derome P, Guiot G (1978) Thalamic spatial variability and the surgical results of lesions placed with neurophysiologic control. Surg Neurol 9(5):307–315
Wharen RE, Okun MS, Guthrie BL, Uitti RJ, Larson P, Foote K et al (2017) Thalamic DBS with a constant-current device in essential tremor: a controlled clinical trial. Parkinsonism Relat Disord 40:18–26. https://doi.org/10.1016/j.parkreldis.2017.03.017
Chen T, Mirzadeh Z, Chapple K, Lambert M, Dhall R, Ponce FA (2016) “Asleep” deep brain stimulation for essential tremor. J Neurosurg 124(6):1842–1849. https://doi.org/10.3171/2015.6.JNS15526
Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW (2007) Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? NeuroImage 34(1):144–155. https://doi.org/10.1016/j.neuroimage.2006.09.018
Traynor C, Heckemann RA, Hammers A, O'Muircheartaigh J, Crum WR, Barker GJ, Richardson MP (2010) Reproducibility of thalamic segmentation based on probabilistic tractography. NeuroImage 52(1):69–85. https://doi.org/10.1016/j.neuroimage.2010.04.024
Herzog J, Hamel W, Wenzelburger R, Potter M, Pinsker MO, Bartussek J et al (2007) Kinematic analysis of thalamic versus subthalamic neurostimulation in postural and intention tremor. Brain 130(Pt 6):1608–1625. https://doi.org/10.1093/brain/awm077
Yamamoto T, Katayama Y, Kano T, Kobayashi K, Oshima H, Fukaya C (2004) Deep brain stimulation for the treatment of parkinsonian, essential, and poststroke tremor: a suitable stimulation method and changes in effective stimulation intensity. J Neurosurg 101(2):201–209. https://doi.org/10.3171/jns.2004.101.2.0201
Ramirez-Zamora A, Okun MS (2016) Deep brain stimulation for the treatment of uncommon tremor syndromes. Expert Rev Neurother 16(8):983–997. https://doi.org/10.1080/14737175.2016.1194756
Papavassiliou E, Rau G, Heath S, Abosch A, Barbaro NM, Larson PS, Lamborn K, Starr PA (2004) Thalamic deep brain stimulation for essential tremor: relation of lead location to outcome. Neurosurgery 54(5):1120–1129; discussion 9-30. https://doi.org/10.1227/01.NEU.0000119329.66931.9E
Oyama G, Foote KD, Hwynn N, Jacobson CE, Malaty IA, Rodriguez RL et al (2011) Rescue leads: a salvage technique for selected patients with a suboptimal response to standard DBS therapy. Parkinsonism Relat Disord 17(6):451–455. https://doi.org/10.1016/j.parkreldis.2011.03.009
Yu H, Hedera P, Fang J, Davis TL, Konrad PE (2009) Confined stimulation using dual thalamic deep brain stimulation leads rescues refractory essential tremor: report of three cases. Stereotact Funct Neurosurg 87(5):309–313. https://doi.org/10.1159/000230694
Servello D, Sassi M, Brambilla A, Porta M, Haq I, Foote KD, Okun MS (2009) De novo and rescue DBS leads for refractory Tourette syndrome patients with severe comorbid OCD: a multiple case report. J Neurol 256(9):1533–1539. https://doi.org/10.1007/s00415-009-5159-6
Pouratian N, Zheng Z, Bari AA, Behnke E, Elias WJ, Desalles AA (2011) Multi-institutional evaluation of deep brain stimulation targeting using probabilistic connectivity-based thalamic segmentation. J Neurosurg 115(5):995–1004. https://doi.org/10.3171/2011.7.JNS11250
Behrens TE, Johansen-Berg H, Woolrich MW, Smith SM, Wheeler-Kingshott CA, Boulby PA et al (2003) Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 6(7):750–757. https://doi.org/10.1038/nn1075
Elias WJ, Zheng ZA, Domer P, Quigg M, Pouratian N (2012) Validation of connectivity-based thalamic segmentation with direct electrophysiologic recordings from human sensory thalamus. NeuroImage 59(3):2025–2034. https://doi.org/10.1016/j.neuroimage.2011.10.049
Kim W, Chivukula S, Hauptman J, Pouratian N (2016) Diffusion tensor imaging-based thalamic segmentation in deep brain stimulation for chronic pain conditions. Stereotact Funct Neurosurg 94(4):225–234. https://doi.org/10.1159/000448079
Rabie A, Verhagen Metman L, Slavin KV (2016) Using “functional” target coordinates of the subthalamic nucleus to assess the indirect and direct methods of the preoperative planning: do the anatomical and functional targets coincide? Brain Sci 6(4):65. https://doi.org/10.3390/brainsci6040065
Henderson JM (2012) “Connectomic surgery”: diffusion tensor imaging (DTI) tractography as a targeting modality for surgical modulation of neural networks. Front Integr Neurosci 6:15
Coenen VA, Varkuti B, Parpaley Y, Skodda S, Prokop T, Urbach H, Li M, Reinacher PC (2017) Postoperative neuroimaging analysis of DRT deep brain stimulation revision surgery for complicated essential tremor. Acta Neurochir 159(5):779–787. https://doi.org/10.1007/s00701-017-3134-z
Sammartino F, Krishna V, King NK, Lozano AM, Schwartz ML, Huang Y et al (2016) Tractography-based ventral intermediate nucleus targeting: novel methodology and intraoperative validation. Mov Disord 31(8):1217–1225. https://doi.org/10.1002/mds.26633
Acknowledgements
Data were provided in part by the Human Connectome Project, the WU-Minn Consortium (Principal Investigators: David Van Essen and Kamil Ugurbil; 1U54MH091657), funded by the 16 NIH Institutes and Centers that support the NIH Blueprint for Neuroscience Research, and by the McDonnell Center for Systems Neuroscience at Washington University.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding
No funding was received for this study.
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed consent
Informed consent was obtained from all individual participants included in the study in accordance with the Human Connectome Project as part of the open source dataset utilized in this study.
Additional information
This study was presented as an oral presentation in abstract form at the 2017 American Society of Functional Neuroradiology meeting in October 2017.
Rights and permissions
About this article
Cite this article
Middlebrooks, E.H., Holanda, V.M., Tuna, I.S. et al. A method for pre-operative single-subject thalamic segmentation based on probabilistic tractography for essential tremor deep brain stimulation. Neuroradiology 60, 303–309 (2018). https://doi.org/10.1007/s00234-017-1972-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00234-017-1972-2