L Okromelidze1, T Tsuboi2, R S Eisinger2, M R Burns2, M Charbel3, M Rana4, S S Grewal2, C-Q Lu1, L Almeida3, K D Foote3, M S Okun2, E H Middlebrooks5,2. 1. From the Departments of Radiology (L.O., C.-Q.L., E.H.M.) and Neurosurgery (S.S.G., E.H.M.), Mayo Clinic, Jacksonville, Florida. 2. Department of Neurology (T.T., R.S.E., M.R.B., L.A., K.D.F., M.S.O.), Norman Fixel Institute for Neurological Diseases. 3. Department of Neurosurgery (K.D.F.), and J. Crayton Pruitt Family Department of Biomedical Engineering (M.C.), University of Florida, Gainesville, Florida. 4. Institute of Medical Psychology and Behavioural Neurobiology (M.R.), University of Tübingen, Tübingen, Germany. 5. From the Departments of Radiology (L.O., C.-Q.L., E.H.M.) and Neurosurgery (S.S.G., E.H.M.), Mayo Clinic, Jacksonville, Florida middlebrooks.erik@mayo.edu.
Abstract
BACKGROUND AND PURPOSE: Deep brain stimulation is a well-established treatment for generalized dystonia, but outcomes remain variable. Establishment of an imaging marker to guide device targeting and programming could possibly impact the efficacy of deep brain stimulation in dystonia, particularly in the absence of acute clinical markers to indicate benefit. We hypothesize that the stimulation-based functional and structural connectivity using resting-state fMRI and DTI can predict therapeutic outcomes in patients with generalized dystonia and deep brain stimulation. MATERIALS AND METHODS: We performed a retrospective analysis of 39 patients with inherited or idiopathic-isolated generalized dystonia who underwent bilateral globus pallidus internus deep brain stimulation. After electrode localization, the volumes of tissue activated were modeled and used as seed regions for functional and structural connectivity measures using a normative data base. Resulting connectivity maps were correlated with postoperative improvement in the Unified Dystonia Rating Scale score. RESULTS: Structural connectivity between the volumes of tissue activated and the primary sensorimotor cortex was correlated with Unified Dystonia Rating Scale improvement, while more anterior prefrontal connectivity was inversely correlated with Unified Dystonia Rating Scale improvement. Functional connectivity between the volumes of tissue activated and primary sensorimotor regions, motor thalamus, and cerebellum was most correlated with Unified Dystonia Rating Scale improvement; however, an inverse correlation with Unified Dystonia Rating Scale improvement was seen in the supplemental motor area and premotor cortex. CONCLUSIONS: Functional and structural connectivity with multiple nodes of the motor network is associated with motor improvement in patients with generalized dystonia undergoing deep brain stimulation. Results from this study may serve as a basis for future development of clinical markers to guide deep brain stimulation targeting and programming in dystonia.
BACKGROUND AND PURPOSE: Deep brain stimulation is a well-established treatment for generalized dystonia, but outcomes remain variable. Establishment of an imaging marker to guide device targeting and programming could possibly impact the efficacy of deep brain stimulation in dystonia, particularly in the absence of acute clinical markers to indicate benefit. We hypothesize that the stimulation-based functional and structural connectivity using resting-state fMRI and DTI can predict therapeutic outcomes in patients with generalized dystonia and deep brain stimulation. MATERIALS AND METHODS: We performed a retrospective analysis of 39 patients with inherited or idiopathic-isolated generalized dystonia who underwent bilateral globus pallidus internus deep brain stimulation. After electrode localization, the volumes of tissue activated were modeled and used as seed regions for functional and structural connectivity measures using a normative data base. Resulting connectivity maps were correlated with postoperative improvement in the Unified Dystonia Rating Scale score. RESULTS: Structural connectivity between the volumes of tissue activated and the primary sensorimotor cortex was correlated with Unified Dystonia Rating Scale improvement, while more anterior prefrontal connectivity was inversely correlated with Unified Dystonia Rating Scale improvement. Functional connectivity between the volumes of tissue activated and primary sensorimotor regions, motor thalamus, and cerebellum was most correlated with Unified Dystonia Rating Scale improvement; however, an inverse correlation with Unified Dystonia Rating Scale improvement was seen in the supplemental motor area and premotor cortex. CONCLUSIONS: Functional and structural connectivity with multiple nodes of the motor network is associated with motor improvement in patients with generalized dystonia undergoing deep brain stimulation. Results from this study may serve as a basis for future development of clinical markers to guide deep brain stimulation targeting and programming in dystonia.
Authors: Bettina Balint; Niccolò E Mencacci; Enza Maria Valente; Antonio Pisani; John Rothwell; Joseph Jankovic; Marie Vidailhet; Kailash P Bhatia Journal: Nat Rev Dis Primers Date: 2018-09-20 Impact factor: 52.329
Authors: Tyler Cheung; Angela M Noecker; Ron L Alterman; Cameron C McIntyre; Michele Tagliati Journal: Ann Neurol Date: 2014-06-18 Impact factor: 10.422
Authors: K A M Pauls; P J Bröckelmann; S Hammesfahr; J Becker; A Hellerbach; V Visser-Vandewalle; T A Dembek; I G Meister; L Timmermann Journal: Parkinsonism Relat Disord Date: 2017-11-07 Impact factor: 4.891
Authors: Jens Volkmann; Alexander Wolters; Andreas Kupsch; Jörg Müller; Andrea A Kühn; Gerd-Helge Schneider; Werner Poewe; Sascha Hering; Wilhelm Eisner; Jan-Uwe Müller; Günther Deuschl; Marcus O Pinsker; Inger-Marie Skogseid; Geir Ketil Roeste; Martin Krause; Volker Tronnier; Alfons Schnitzler; Jürgen Voges; Guido Nikkhah; Jan Vesper; Joseph Classen; Markus Naumann; Reiner Benecke Journal: Lancet Neurol Date: 2012-11-01 Impact factor: 44.182
Authors: E Moro; C LeReun; J K Krauss; A Albanese; J-P Lin; S Walleser Autiero; T C Brionne; M Vidailhet Journal: Eur J Neurol Date: 2017-02-10 Impact factor: 6.089
Authors: Andres M Lozano; Nir Lipsman; Hagai Bergman; Peter Brown; Stephan Chabardes; Jin Woo Chang; Keith Matthews; Cameron C McIntyre; Thomas E Schlaepfer; Michael Schulder; Yasin Temel; Jens Volkmann; Joachim K Krauss Journal: Nat Rev Neurol Date: 2019-03 Impact factor: 42.937
Authors: E H Middlebrooks; R A Domingo; T Vivas-Buitrago; L Okromelidze; T Tsuboi; J K Wong; R S Eisinger; L Almeida; M R Burns; A Horn; R J Uitti; R E Wharen; V M Holanda; S S Grewal Journal: AJNR Am J Neuroradiol Date: 2020-08-13 Impact factor: 3.825
Authors: Vinata Vedam-Mai; Karl Deisseroth; James Giordano; Gabriel Lazaro-Munoz; Winston Chiong; Nanthia Suthana; Jean-Philippe Langevin; Jay Gill; Wayne Goodman; Nicole R Provenza; Casey H Halpern; Rajat S Shivacharan; Tricia N Cunningham; Sameer A Sheth; Nader Pouratian; Katherine W Scangos; Helen S Mayberg; Andreas Horn; Kara A Johnson; Christopher R Butson; Ro'ee Gilron; Coralie de Hemptinne; Robert Wilt; Maria Yaroshinsky; Simon Little; Philip Starr; Greg Worrell; Prasad Shirvalkar; Edward Chang; Jens Volkmann; Muthuraman Muthuraman; Sergiu Groppa; Andrea A Kühn; Luming Li; Matthew Johnson; Kevin J Otto; Robert Raike; Steve Goetz; Chengyuan Wu; Peter Silburn; Binith Cheeran; Yagna J Pathak; Mahsa Malekmohammadi; Aysegul Gunduz; Joshua K Wong; Stephanie Cernera; Wei Hu; Aparna Wagle Shukla; Adolfo Ramirez-Zamora; Wissam Deeb; Addie Patterson; Kelly D Foote; Michael S Okun Journal: Front Hum Neurosci Date: 2021-04-19 Impact factor: 3.169
Authors: Brandon L Brown; Rachel M Zalla; Courtney T Shepard; Russell M Howard; Jonathan A Kopechek; David S K Magnuson; Scott R Whittemore Journal: Front Neuroanat Date: 2021-03-22 Impact factor: 3.856
Authors: Marenka Smit; Alberto Albanese; Monika Benson; Mark J Edwards; Holm Graessner; Michael Hutchinson; Robert Jech; Joachim K Krauss; Francesca Morgante; Belen Pérez Dueñas; Richard B Reilly; Michele Tinazzi; Maria Fiorella Contarino; Marina A J Tijssen Journal: Front Neurol Date: 2021-06-03 Impact factor: 4.003