Mapping dysfunctional circuits in the frontal cortex using deep brain stimulation

Barbara Hollunder; Jill L. Ostrem; Ilkem Aysu Sahin; Nanditha Rajamani; Simón Oxenford; Konstantin Butenko; Clemens Neudorfer; Pablo Reinhardt; Patricia Zvarova; Mircea Polosan; Harith Akram; Matteo Vissani; Chencheng Zhang; Bomin Sun; Pavel Navratil; Martin M. Reich; Jens Volkmann; Fang Cheng Yeh; Juan Carlos Baldermann; Till A. Dembek; Veerle Visser-Vandewalle; Eduardo Joaquim Lopes Alho; Paulo Roberto Franceschini; Pranav Nanda; Carsten Finke; Andrea A. Kühn; Darin D. Dougherty; R. Mark Richardson; Hagai Bergman; Mahlon R. DeLong; Alberto Mazzoni; Luigi M. Romito; Himanshu Tyagi; Ludvic Zrinzo; Eileen M. Joyce; Stephan Chabardes; Philip A. Starr; Ningfei Li; Andreas Horn

doi:10.1038/s41593-024-01570-1

Mapping dysfunctional circuits in the frontal cortex using deep brain stimulation

Barbara Hollunder, Jill L. Ostrem, Ilkem Aysu Sahin, Nanditha Rajamani, Simón Oxenford, Konstantin Butenko, Clemens Neudorfer, Pablo Reinhardt, Patricia Zvarova, Mircea Polosan, Harith Akram, Matteo Vissani, Chencheng Zhang, Bomin Sun, Pavel Navratil, Martin M. Reich, Jens Volkmann, Fang Cheng Yeh, Juan Carlos Baldermann, Till A. DembekVeerle Visser-Vandewalle, Eduardo Joaquim Lopes Alho, Paulo Roberto Franceschini, Pranav Nanda, Carsten Finke, Andrea A. Kühn, Darin D. Dougherty, R. Mark Richardson, Hagai Bergman, Mahlon R. DeLong, Alberto Mazzoni, Luigi M. Romito, Himanshu Tyagi, Ludvic Zrinzo, Eileen M. Joyce, Stephan Chabardes, Philip A. Starr, Ningfei Li^*, Andreas Horn^*

^*Corresponding author for this work

Edmond & Lily Safra Center for Brain Sciences

Research output: Contribution to journal › Article › peer-review

13 Scopus citations

Abstract

Frontal circuits play a critical role in motor, cognitive and affective processing, and their dysfunction may result in a variety of brain disorders. However, exactly which frontal domains mediate which (dys)functions remains largely elusive. We studied 534 deep brain stimulation electrodes implanted to treat four different brain disorders. By analyzing which connections were modulated for optimal therapeutic response across these disorders, we segregated the frontal cortex into circuits that had become dysfunctional in each of them. Dysfunctional circuits were topographically arranged from occipital to frontal, ranging from interconnections with sensorimotor cortices in dystonia, the primary motor cortex in Tourette’s syndrome, the supplementary motor area in Parkinson’s disease, to ventromedial prefrontal and anterior cingulate cortices in obsessive-compulsive disorder. Our findings highlight the integration of deep brain stimulation with brain connectomics as a powerful tool to explore couplings between brain structure and functional impairments in the human brain.

Original language	English
Pages (from-to)	573-586
Number of pages	14
Journal	Nature Neuroscience
Volume	27
Issue number	3
DOIs	https://doi.org/10.1038/s41593-024-01570-1
State	Published - Mar 2024

Bibliographical note

Publisher Copyright:
© The Author(s) 2024.

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Hollunder, B., Ostrem, J. L., Sahin, I. A., Rajamani, N., Oxenford, S., Butenko, K., Neudorfer, C., Reinhardt, P., Zvarova, P., Polosan, M., Akram, H., Vissani, M., Zhang, C., Sun, B., Navratil, P., Reich, M. M., Volkmann, J., Yeh, F. C., Baldermann, J. C., ... Horn, A. (2024). Mapping dysfunctional circuits in the frontal cortex using deep brain stimulation. Nature Neuroscience, 27(3), 573-586. https://doi.org/10.1038/s41593-024-01570-1

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title = "Mapping dysfunctional circuits in the frontal cortex using deep brain stimulation",

abstract = "Frontal circuits play a critical role in motor, cognitive and affective processing, and their dysfunction may result in a variety of brain disorders. However, exactly which frontal domains mediate which (dys)functions remains largely elusive. We studied 534 deep brain stimulation electrodes implanted to treat four different brain disorders. By analyzing which connections were modulated for optimal therapeutic response across these disorders, we segregated the frontal cortex into circuits that had become dysfunctional in each of them. Dysfunctional circuits were topographically arranged from occipital to frontal, ranging from interconnections with sensorimotor cortices in dystonia, the primary motor cortex in Tourette{\textquoteright}s syndrome, the supplementary motor area in Parkinson{\textquoteright}s disease, to ventromedial prefrontal and anterior cingulate cortices in obsessive-compulsive disorder. Our findings highlight the integration of deep brain stimulation with brain connectomics as a powerful tool to explore couplings between brain structure and functional impairments in the human brain.",

author = "Barbara Hollunder and Ostrem, {Jill L.} and Sahin, {Ilkem Aysu} and Nanditha Rajamani and Sim{\'o}n Oxenford and Konstantin Butenko and Clemens Neudorfer and Pablo Reinhardt and Patricia Zvarova and Mircea Polosan and Harith Akram and Matteo Vissani and Chencheng Zhang and Bomin Sun and Pavel Navratil and Reich, {Martin M.} and Jens Volkmann and Yeh, {Fang Cheng} and Baldermann, {Juan Carlos} and Dembek, {Till A.} and Veerle Visser-Vandewalle and Alho, {Eduardo Joaquim Lopes} and Franceschini, {Paulo Roberto} and Pranav Nanda and Carsten Finke and K{\"u}hn, {Andrea A.} and Dougherty, {Darin D.} and Richardson, {R. Mark} and Hagai Bergman and DeLong, {Mahlon R.} and Alberto Mazzoni and Romito, {Luigi M.} and Himanshu Tyagi and Ludvic Zrinzo and Joyce, {Eileen M.} and Stephan Chabardes and Starr, {Philip A.} and Ningfei Li and Andreas Horn",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2024.",

year = "2024",

month = mar,

doi = "10.1038/s41593-024-01570-1",

language = "אנגלית",

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Hollunder, B, Ostrem, JL, Sahin, IA, Rajamani, N, Oxenford, S, Butenko, K, Neudorfer, C, Reinhardt, P, Zvarova, P, Polosan, M, Akram, H, Vissani, M, Zhang, C, Sun, B, Navratil, P, Reich, MM, Volkmann, J, Yeh, FC, Baldermann, JC, Dembek, TA, Visser-Vandewalle, V, Alho, EJL, Franceschini, PR, Nanda, P, Finke, C, Kühn, AA, Dougherty, DD, Richardson, RM, Bergman, H, DeLong, MR, Mazzoni, A, Romito, LM, Tyagi, H, Zrinzo, L, Joyce, EM, Chabardes, S, Starr, PA, Li, N & Horn, A 2024, 'Mapping dysfunctional circuits in the frontal cortex using deep brain stimulation', Nature Neuroscience, vol. 27, no. 3, pp. 573-586. https://doi.org/10.1038/s41593-024-01570-1

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AU - Hollunder, Barbara

AU - Ostrem, Jill L.

AU - Sahin, Ilkem Aysu

AU - Rajamani, Nanditha

AU - Oxenford, Simón

AU - Butenko, Konstantin

AU - Neudorfer, Clemens

AU - Reinhardt, Pablo

AU - Zvarova, Patricia

AU - Polosan, Mircea

AU - Akram, Harith

AU - Vissani, Matteo

AU - Zhang, Chencheng

AU - Sun, Bomin

AU - Navratil, Pavel

AU - Reich, Martin M.

AU - Volkmann, Jens

AU - Yeh, Fang Cheng

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AU - Dembek, Till A.

AU - Visser-Vandewalle, Veerle

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AU - DeLong, Mahlon R.

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AU - Romito, Luigi M.

AU - Tyagi, Himanshu

AU - Zrinzo, Ludvic

AU - Joyce, Eileen M.

AU - Chabardes, Stephan

AU - Starr, Philip A.

AU - Li, Ningfei

AU - Horn, Andreas

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Mapping dysfunctional circuits in the frontal cortex using deep brain stimulation

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