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Research ArticleFunctional

Connectomic Basis for Tremor Control in Stereotactic Radiosurgical Thalamotomy

E.H. Middlebrooks, R.A. Popple, E. Greco, L. Okromelidze, H.C. Walker, D.A. Lakhani, A.R. Anderson, E.M. Thomas, H.D. Deshpande, B.A. McCullough, N.P. Stover, V.W. Sung, A.P. Nicholas, D.G. Standaert, T. Yacoubian, M.N. Dean, J.A. Roper, S.S. Grewal, M.T. Holland, J.N. Bentley, B.L. Guthrie and M. Bredel
American Journal of Neuroradiology February 2023, 44 (2) 157-164; DOI: https://doi.org/10.3174/ajnr.A7778
E.H. Middlebrooks
aFrom the Departments of Radiology (E.H.M., E.G., L.O., D.A.L.)
bNeurosurgery (E.H.M., S.S.G.), Mayo Clinic, Jacksonville, Florida
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R.A. Popple
cDepartments of Radiation Oncology (R.A.P., A.R.A., E.M.T., M.B.)
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E. Greco
aFrom the Departments of Radiology (E.H.M., E.G., L.O., D.A.L.)
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L. Okromelidze
aFrom the Departments of Radiology (E.H.M., E.G., L.O., D.A.L.)
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H.C. Walker
dNeurology (H.C.W., B.A.M., N.P.S., V.W.S., A.P.N., D.G.S., T.Y., M.N.D.)
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D.A. Lakhani
aFrom the Departments of Radiology (E.H.M., E.G., L.O., D.A.L.)
gDepartment of Radiology (D.A.L.), West Virginia University, Morgantown, West Virginia
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  • ORCID record for D.A. Lakhani
A.R. Anderson
cDepartments of Radiation Oncology (R.A.P., A.R.A., E.M.T., M.B.)
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E.M. Thomas
cDepartments of Radiation Oncology (R.A.P., A.R.A., E.M.T., M.B.)
hDepartment of Radiation Oncology (E.M.T.), Ohio State University, Columbus, Ohio
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H.D. Deshpande
eRadiology (H.D.D.)
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B.A. McCullough
dNeurology (H.C.W., B.A.M., N.P.S., V.W.S., A.P.N., D.G.S., T.Y., M.N.D.)
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N.P. Stover
dNeurology (H.C.W., B.A.M., N.P.S., V.W.S., A.P.N., D.G.S., T.Y., M.N.D.)
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V.W. Sung
dNeurology (H.C.W., B.A.M., N.P.S., V.W.S., A.P.N., D.G.S., T.Y., M.N.D.)
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A.P. Nicholas
dNeurology (H.C.W., B.A.M., N.P.S., V.W.S., A.P.N., D.G.S., T.Y., M.N.D.)
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D.G. Standaert
dNeurology (H.C.W., B.A.M., N.P.S., V.W.S., A.P.N., D.G.S., T.Y., M.N.D.)
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T. Yacoubian
dNeurology (H.C.W., B.A.M., N.P.S., V.W.S., A.P.N., D.G.S., T.Y., M.N.D.)
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M.N. Dean
dNeurology (H.C.W., B.A.M., N.P.S., V.W.S., A.P.N., D.G.S., T.Y., M.N.D.)
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J.A. Roper
iSchool of Kinesiology (J.A.R.), Auburn University, Auburn, Alabama
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S.S. Grewal
bNeurosurgery (E.H.M., S.S.G.), Mayo Clinic, Jacksonville, Florida
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M.T. Holland
fNeurosurgery (M.T.H., J.N.B., B.L.G.), University of Alabama at Birmingham, Birmingham, Alabama
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J.N. Bentley
fNeurosurgery (M.T.H., J.N.B., B.L.G.), University of Alabama at Birmingham, Birmingham, Alabama
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B.L. Guthrie
fNeurosurgery (M.T.H., J.N.B., B.L.G.), University of Alabama at Birmingham, Birmingham, Alabama
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M. Bredel
cDepartments of Radiation Oncology (R.A.P., A.R.A., E.M.T., M.B.)
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Abstract

BACKGROUND AND PURPOSE: Given the increased use of stereotactic radiosurgical thalamotomy and other ablative therapies for tremor, new biomarkers are needed to improve outcomes. Using resting-state fMRI and MR tractography, we hypothesized that a “connectome fingerprint” can predict tremor outcomes and potentially serve as a targeting biomarker for stereotactic radiosurgical thalamotomy.

MATERIALS AND METHODS: We evaluated 27 patients who underwent unilateral stereotactic radiosurgical thalamotomy for essential tremor or tremor-predominant Parkinson disease. Percentage postoperative improvement in the contralateral limb Fahn‐Tolosa‐Marin Clinical Tremor Rating Scale (TRS) was the primary end point. Connectome-style resting-state fMRI and MR tractography were performed before stereotactic radiosurgery. Using the final lesion volume as a seed, “connectivity fingerprints” representing ideal connectivity maps were generated as whole-brain R-maps using a voxelwise nonparametric Spearman correlation. A leave-one-out cross-validation was performed using the generated R-maps.

RESULTS: The mean improvement in the contralateral tremor score was 55.1% (SD, 38.9%) at a mean follow-up of 10.0 (SD, 5.0) months. Structural connectivity correlated with contralateral TRS improvement (r = 0.52; P  = .006) and explained 27.0% of the variance in outcome. Functional connectivity correlated with contralateral TRS improvement (r = 0.50; P  = .008) and explained 25.0% of the variance in outcome. Nodes most correlated with tremor improvement corresponded to areas of known network dysfunction in tremor, including the cerebello-thalamo-cortical pathway and the primary and extrastriate visual cortices.

CONCLUSIONS: Stereotactic radiosurgical targets with a distinct connectivity profile predict improvement in tremor after treatment. Such connectomic fingerprints show promise for developing patient-specific biomarkers to guide therapy with stereotactic radiosurgical thalamotomy.

ABBREVIATIONS:

BOLD
blood oxygen level–dependent MRI
DBS
deep brain stimulation
DRTT
dentato-rubro-thalamic tract
SMS
simultaneous multislice
SRS
stereotactic radiosurgery
TRS
Fahn‐Tolosa‐Marin Clinical Tremor Rating Scale
VIM
ventral intermediate nucleus
  • © 2023 by American Journal of Neuroradiology
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American Journal of Neuroradiology: 44 (2)
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Connectomic Basis for Tremor Control in Stereotactic Radiosurgical Thalamotomy
E.H. Middlebrooks, R.A. Popple, E. Greco, L. Okromelidze, H.C. Walker, D.A. Lakhani, A.R. Anderson, E.M. Thomas, H.D. Deshpande, B.A. McCullough, N.P. Stover, V.W. Sung, A.P. Nicholas, D.G. Standaert, T. Yacoubian, M.N. Dean, J.A. Roper, S.S. Grewal, M.T. Holland, J.N. Bentley, B.L. Guthrie, M. Bredel
American Journal of Neuroradiology Feb 2023, 44 (2) 157-164; DOI: 10.3174/ajnr.A7778

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Connectomic Basis for Tremor Control in Stereotactic Radiosurgical Thalamotomy
E.H. Middlebrooks, R.A. Popple, E. Greco, L. Okromelidze, H.C. Walker, D.A. Lakhani, A.R. Anderson, E.M. Thomas, H.D. Deshpande, B.A. McCullough, N.P. Stover, V.W. Sung, A.P. Nicholas, D.G. Standaert, T. Yacoubian, M.N. Dean, J.A. Roper, S.S. Grewal, M.T. Holland, J.N. Bentley, B.L. Guthrie, M. Bredel
American Journal of Neuroradiology Feb 2023, 44 (2) 157-164; DOI: 10.3174/ajnr.A7778
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