Stimulation of the Presupplementary Motor Area Cluster of the Subthalamic Nucleus Predicts More Consistent Clinical Outcomes.
Journal
Neurosurgery
ISSN: 1524-4040
Titre abrégé: Neurosurgery
Pays: United States
ID NLM: 7802914
Informations de publication
Date de publication:
01 05 2023
01 05 2023
Historique:
received:
19
07
2022
accepted:
05
10
2022
medline:
19
4
2023
pubmed:
27
1
2023
entrez:
26
1
2023
Statut:
ppublish
Résumé
The development of diffusion tensor imaging and tractography has raised increasing interest in the functional targeting of deep brain stimulation of the subthalamic nucleus (STN) in Parkinson disease. To study, using deterministic tractography, the functional subdivisions of the STN and hyperdirect white matter connections located between the STN and the medial frontal cortex, especially the presupplementary motor area (preSMA), SMA, primary motor area (M1), and dorsolateral premotor cortex, and to study retrospectively whether this information correlates with clinical outcome. Twenty-two patients with Parkinson disease who underwent STN deep brain stimulation were analyzed. Using 3 T MR images, the medial frontal cortex was manually segmented into preSMA, SMA, M1, and dorsolateral premotor cortex, which were then used to determine the functional subdivisions of the lateral border of the STN. The intersectional quantities of the volume of activated tissue (VAT) and the hyperdirect white matter connections were calculated. The results were combined with clinical data including unilateral 12-month postoperative motor outcome and levodopa equivalent daily dose. Stimulated clusters of the STN were connected mostly to the cortical SMA and preSMA regions. Patients with primarily preSMA cluster stimulation (presmaVAT% ≥ 50%) had good responses to the treatment with unilateral motor improvement over 40% and levodopa equivalent daily dose reduction over 60%. Larger VAT was not found to correlate with better patient outcomes. Our study is the first to suggest that stimulating, predominantly, the STN cluster where preSMA hyperdirect pathways are located, could be predictive of more consistent treatment results.
Sections du résumé
BACKGROUND
The development of diffusion tensor imaging and tractography has raised increasing interest in the functional targeting of deep brain stimulation of the subthalamic nucleus (STN) in Parkinson disease.
OBJECTIVE
To study, using deterministic tractography, the functional subdivisions of the STN and hyperdirect white matter connections located between the STN and the medial frontal cortex, especially the presupplementary motor area (preSMA), SMA, primary motor area (M1), and dorsolateral premotor cortex, and to study retrospectively whether this information correlates with clinical outcome.
METHODS
Twenty-two patients with Parkinson disease who underwent STN deep brain stimulation were analyzed. Using 3 T MR images, the medial frontal cortex was manually segmented into preSMA, SMA, M1, and dorsolateral premotor cortex, which were then used to determine the functional subdivisions of the lateral border of the STN. The intersectional quantities of the volume of activated tissue (VAT) and the hyperdirect white matter connections were calculated. The results were combined with clinical data including unilateral 12-month postoperative motor outcome and levodopa equivalent daily dose.
RESULTS
Stimulated clusters of the STN were connected mostly to the cortical SMA and preSMA regions. Patients with primarily preSMA cluster stimulation (presmaVAT% ≥ 50%) had good responses to the treatment with unilateral motor improvement over 40% and levodopa equivalent daily dose reduction over 60%. Larger VAT was not found to correlate with better patient outcomes.
CONCLUSION
Our study is the first to suggest that stimulating, predominantly, the STN cluster where preSMA hyperdirect pathways are located, could be predictive of more consistent treatment results.
Identifiants
pubmed: 36700693
doi: 10.1227/neu.0000000000002292
pii: 00006123-202305000-00020
doi:
Substances chimiques
Levodopa
46627O600J
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1058-1065Informations de copyright
Copyright © Congress of Neurological Surgeons 2022. All rights reserved.
Références
Limousin P, Krack P, Pollak P, et al. Electrical stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med. 1998;339(16):1105-1111.
Benabid AL, Krack PP, Benazzouz A, et al. Deep brain stimulation of the subthalamic nucleus for Parkinson's disease: methodologic aspects and clinical criteria. Neurology. 2000;55(12 suppl 6):S40-S44.
Kleiner-Fisman G, Herzog J, Fisman DN, et al. Subthalamic nucleus deep brain stimulation: summary and meta-analysis of outcomes. Mov Disord. 2006;21(suppl 14):290-304.
Bronstein JM, Tagliati M, Alterman RL, et al. Deep brain stimulation for Parkinson disease: an expert consensus and review of key issues. Arch Neurol. 2011;68(2):165.
Krack P, Volkmann J, Tinkhauser G, et al. Deep brain stimulation in movement disorders: from experimental surgery to evidence-based therapy. Mov Disord. 2019;34(12):1795-1810.
Schaltenbrand G, Wahren WSchaltenbrand and Wahren’s Atlas for Stereotaxy of the Human Brain, 2nd ed. Thieme; 1977.
Talairach J, Tournoux PTalairach and Tournoux’s Co-Planar Stereotaxic Atlas of the Human Brain, 1st ed. Thieme; 1988.
Aziz TZ, Nandi D, Parkin S, et al. Targeting the subthalamic nucleus. Stereotact Funct Neurosurg. 2001;77(1-4):87-90.
Patel NK, Heywood P, O'Sullivan K, Love S, Gill SS. MRI-directed subthalamic nucleus surgery for Parkinson's disease. Stereotact Funct Neurosurg. 2002;78(3-4):132-145.
Patel NK, Khan S, Gill SS. Comparison of atlas- and magnetic-resonance-imaging-based stereotactic targeting of the subthalamic nucleus in the surgical treatment of Parkinson's disease. Stereotact Funct Neurosurg. 2008;86(3):153-161.
Lahtinen M, Haapaniemi T, Kauppinen M, et al. A comparison of indirect and direct targeted STN DBS in the treatment of Parkinson's disease-surgical method and clinical outcome over 15-year timespan. Acta Neurochir (Wien). 2020;162(5):1067-1076.
Longhi M, Ricciardi G, Tommasi G, et al. The role of 3T magnetic resonance imaging for targeting the human subthalamic nucleus in deep brain stimulation for Parkinson disease. J Neurol Surg A Cent Eur Neurosurg. 2015;76(3):181-189.
Alkemade A, Forstmann B. Imaging of the human subthalamic nucleus. Handb Clin Neurol. 2021;180(5):403-416.
den Dunnen WF, Staal MJ. Anatomical alterations of the subthalamic nucleus in relation to age: a postmortem study. Mov Disord. 2005;20(7):893-898.
Daniluk S, Davies K, Ellias SA, et al. Assessment of the variability in the anatomical position and size of the subthalamic nucleus among patients with advanced Parkinson's disease using magnetic resonance imaging. Acta Neurochir (Wien). 2010;152(2):201-210.
Patriat R, Niederer J, Kaplan J, et al. Morphological changes in the subthalamic nucleus of people with mild-to-moderate Parkinson's disease: a 7T MRI study. Sci Rep. 2020;10(1):8785.
Hamel W, Köppen JA, Alesch F, et al. Targeting of the subthalamic nucleus for deep brain stimulation: a survey among Parkinson disease specialists. World Neurosurg. 2017;99:41-46.
Johnsen EL, Sunde N, Mogensen PH, et al. MRI verified STN stimulation site—improvement and clinical outcome. Eur J Neurol. 2010;17(5):746-753.
Welter ML, Schüpbach M, Czernecki V, et al. Optimal target localization for subthalamic stimulation in patients with Parkinson disease. Neurology. 2014;82(15):1352-1361.
Güngör A, Baydın ŞS, Holanda VM, et al. Microsurgical anatomy of the subthalamic nucleus: correlating fiber dissection results with 3-T magnetic resonance imaging using neuronavigation. J Neurosurg. 2018;130(3):716-732.
Akram H, Sotiropoulos SN, Jbabdi S, et al. Subthalamic deep brain stimulation sweet spots and hyperdirect cortical connectivity in Parkinson's disease. Neuroimage. 2017;158(15):332-345.
Coenen VA, Jenkner C, Honey CR, et al. Electrophysiologic validation of diffusion tensor imaging tractography during deep brain stimulation surgery. AJNR Am J Neuroradiol. 2016;37(8):1470-1478.
Lambert C, Zrinzo L, Nagy Z, et al. Confirmation of functional zones within the human subthalamic nucleus: patterns of connectivity and sub-parcellation using diffusion weighted imaging. Neuroimage. 2012;60(1):83-94.
Walker HC, Huang H, Gonzalez CL, et al. Short latency activation of cortex during clinically effective subthalamic deep brain stimulation for Parkinson's disease. Mov Disord. 2012;27(7):864-873.
Miocinovic S, de Hemptinne C, Chen W, et al. Cortical potentials evoked by subthalamic stimulation demonstrate a short latency hyperdirect pathway in humans. J Neurosci. 2018;38(43):9129-9141.
Chen W, de Hemptinne C, Miller AM, et al. Prefrontal-subthalamic hyperdirect pathway modulates movement inhibition in humans. Neuron. 2020;106(4):579-588.e3.
Avecillas-Chasin JM, Alonso-Frech F, Nombela C, et al. Stimulation of the tractography-defined subthalamic nucleus regions correlates with clinical outcomes. Neurosurgery. 2019;85(2):294-303.
Brodmann K. Vergleichende Lokalisationslehre der Großhirnrinde. Barth; 1909.
Ruan J, Bludau S, Palomero-Gallagher N, et al. Cytoarchitecture, probability maps, and functions of the human supplementary and pre-supplementary motor areas. Brain Struct Funct. 2018;223(9):4169-4186.
Dum R, Strick P. Motor areas in the frontal lobe of the primate. Physiol Behav. 2002;77(4-5):677-682.
Kim JH, Lee JM, Jo HJ, et al. Defining functional SMA and pre-SMA subregions in human MFC using resting state fMRI: functional connectivity-based parcellation method. Neuroimage. 2010;49(3):2375-2386.
Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE. Systematic review of levodopa dose equivalency reporting in Parkinson's disease. Mov Disord. 2010;25(15):2649-2653.
Brunenberg EJ, Moeskops P, Backes WH, et al. Structural and resting state functional connectivity of the subthalamic nucleus: identification of motor STN parts and the hyperdirect pathway. PLoS One. 2012;7(6):e39061.
Hamani C, Florence G, Heinsen H, et al. Subthalamic nucleus deep brain stimulation: basic concepts and novel perspectives. eNeuro. 2017;4(5):ENEURO.0140-17.2017.
Nachev P, Kennard C, Husain H. Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci. 2008;9(11):856-869.
Horn A, Reich M, Vorwerk J, et al. Connectivity Predicts deep brain stimulation outcome in Parkinson disease. Ann Neurol. 2017;82(1):67-78.
Prent N, Potters WV, Boon LI, et al. Distance to white matter tracts is associated with deep brain stimulation motor outcome in Parkinson's disease. J Neurosurg. 2020;133(2):433-442.
Mahlknecht P, Akram H, Georgiev D, et al. Pyramidal tract activation due to subthalamic deep brain stimulation in Parkinson's disease. Mov Disord. 2017;32(8):1174-1182.
Vassal F, Dilly D, Boutet C, et al. White matter tracts involved by deep brain stimulation of the subthalamic nucleus in Parkinson's disease: a connectivity study based on preoperative diffusion tensor imaging tractography. Br J Neurosurg. 2020;34(2):187-195.
Petersen M, Lund T, Sunde N, 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):1657-1668.