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Functional correlates of the therapeutic and adverse effects evoked by thalamic stimulation for essential tremor

Deep brain stimulation is an established neurosurgical therapy for movement disorders including essential tremor and Parkinson’s disease. While typically highly effective, deep brain stimulation can sometimes yield suboptimal therapeutic benefit and can cause adverse effects. In this study, we teste...

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Autores principales: Gibson, William S., Jo, Hang Joon, Testini, Paola, Cho, Shinho, Felmlee, Joel P., Welker, Kirk M., Klassen, Bryan T., Min, Hoon-Ki, Lee, Kendall H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4958905/
https://www.ncbi.nlm.nih.gov/pubmed/27329768
http://dx.doi.org/10.1093/brain/aww145
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author Gibson, William S.
Jo, Hang Joon
Testini, Paola
Cho, Shinho
Felmlee, Joel P.
Welker, Kirk M.
Klassen, Bryan T.
Min, Hoon-Ki
Lee, Kendall H.
author_facet Gibson, William S.
Jo, Hang Joon
Testini, Paola
Cho, Shinho
Felmlee, Joel P.
Welker, Kirk M.
Klassen, Bryan T.
Min, Hoon-Ki
Lee, Kendall H.
author_sort Gibson, William S.
collection PubMed
description Deep brain stimulation is an established neurosurgical therapy for movement disorders including essential tremor and Parkinson’s disease. While typically highly effective, deep brain stimulation can sometimes yield suboptimal therapeutic benefit and can cause adverse effects. In this study, we tested the hypothesis that intraoperative functional magnetic resonance imaging could be used to detect deep brain stimulation-evoked changes in functional and effective connectivity that would correlate with the therapeutic and adverse effects of stimulation. Ten patients receiving deep brain stimulation of the ventralis intermedius thalamic nucleus for essential tremor underwent functional magnetic resonance imaging during stimulation applied at a series of stimulation localizations, followed by evaluation of deep brain stimulation-evoked therapeutic and adverse effects. Correlations between the therapeutic effectiveness of deep brain stimulation (3 months postoperatively) and deep brain stimulation-evoked changes in functional and effective connectivity were assessed using region of interest-based correlation analysis and dynamic causal modelling, respectively. Further, we investigated whether brain regions might exist in which activation resulting from deep brain stimulation might correlate with the presence of paraesthesias, the most common deep brain stimulation-evoked adverse effect. Thalamic deep brain stimulation resulted in activation within established nodes of the tremor circuit: sensorimotor cortex, thalamus, contralateral cerebellar cortex and deep cerebellar nuclei (FDR q < 0.05). Stimulation-evoked activation in all these regions of interest, as well as activation within the supplementary motor area, brainstem, and inferior frontal gyrus, exhibited significant correlations with the long-term therapeutic effectiveness of deep brain stimulation (P < 0.05), with the strongest correlation (P < 0.001) observed within the contralateral cerebellum. Dynamic causal modelling revealed a correlation between therapeutic effectiveness and attenuated within-region inhibitory connectivity in cerebellum. Finally, specific subregions of sensorimotor cortex were identified in which deep brain stimulation-evoked activation correlated with the presence of unwanted paraesthesias. These results suggest that thalamic deep brain stimulation in tremor likely exerts its effects through modulation of both olivocerebellar and thalamocortical circuits. In addition, our findings indicate that deep brain stimulation-evoked functional activation maps obtained intraoperatively may contain predictive information pertaining to the therapeutic and adverse effects induced by deep brain stimulation.
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spelling pubmed-49589052016-07-27 Functional correlates of the therapeutic and adverse effects evoked by thalamic stimulation for essential tremor Gibson, William S. Jo, Hang Joon Testini, Paola Cho, Shinho Felmlee, Joel P. Welker, Kirk M. Klassen, Bryan T. Min, Hoon-Ki Lee, Kendall H. Brain Original Articles Deep brain stimulation is an established neurosurgical therapy for movement disorders including essential tremor and Parkinson’s disease. While typically highly effective, deep brain stimulation can sometimes yield suboptimal therapeutic benefit and can cause adverse effects. In this study, we tested the hypothesis that intraoperative functional magnetic resonance imaging could be used to detect deep brain stimulation-evoked changes in functional and effective connectivity that would correlate with the therapeutic and adverse effects of stimulation. Ten patients receiving deep brain stimulation of the ventralis intermedius thalamic nucleus for essential tremor underwent functional magnetic resonance imaging during stimulation applied at a series of stimulation localizations, followed by evaluation of deep brain stimulation-evoked therapeutic and adverse effects. Correlations between the therapeutic effectiveness of deep brain stimulation (3 months postoperatively) and deep brain stimulation-evoked changes in functional and effective connectivity were assessed using region of interest-based correlation analysis and dynamic causal modelling, respectively. Further, we investigated whether brain regions might exist in which activation resulting from deep brain stimulation might correlate with the presence of paraesthesias, the most common deep brain stimulation-evoked adverse effect. Thalamic deep brain stimulation resulted in activation within established nodes of the tremor circuit: sensorimotor cortex, thalamus, contralateral cerebellar cortex and deep cerebellar nuclei (FDR q < 0.05). Stimulation-evoked activation in all these regions of interest, as well as activation within the supplementary motor area, brainstem, and inferior frontal gyrus, exhibited significant correlations with the long-term therapeutic effectiveness of deep brain stimulation (P < 0.05), with the strongest correlation (P < 0.001) observed within the contralateral cerebellum. Dynamic causal modelling revealed a correlation between therapeutic effectiveness and attenuated within-region inhibitory connectivity in cerebellum. Finally, specific subregions of sensorimotor cortex were identified in which deep brain stimulation-evoked activation correlated with the presence of unwanted paraesthesias. These results suggest that thalamic deep brain stimulation in tremor likely exerts its effects through modulation of both olivocerebellar and thalamocortical circuits. In addition, our findings indicate that deep brain stimulation-evoked functional activation maps obtained intraoperatively may contain predictive information pertaining to the therapeutic and adverse effects induced by deep brain stimulation. Oxford University Press 2016-08 2016-06-21 /pmc/articles/PMC4958905/ /pubmed/27329768 http://dx.doi.org/10.1093/brain/aww145 Text en © The Author (2016). Published by Oxford University Press on behalf of the Guarantors of Brain. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Original Articles
Gibson, William S.
Jo, Hang Joon
Testini, Paola
Cho, Shinho
Felmlee, Joel P.
Welker, Kirk M.
Klassen, Bryan T.
Min, Hoon-Ki
Lee, Kendall H.
Functional correlates of the therapeutic and adverse effects evoked by thalamic stimulation for essential tremor
title Functional correlates of the therapeutic and adverse effects evoked by thalamic stimulation for essential tremor
title_full Functional correlates of the therapeutic and adverse effects evoked by thalamic stimulation for essential tremor
title_fullStr Functional correlates of the therapeutic and adverse effects evoked by thalamic stimulation for essential tremor
title_full_unstemmed Functional correlates of the therapeutic and adverse effects evoked by thalamic stimulation for essential tremor
title_short Functional correlates of the therapeutic and adverse effects evoked by thalamic stimulation for essential tremor
title_sort functional correlates of the therapeutic and adverse effects evoked by thalamic stimulation for essential tremor
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4958905/
https://www.ncbi.nlm.nih.gov/pubmed/27329768
http://dx.doi.org/10.1093/brain/aww145
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