Mapping dysfunctional circuits in the frontal cortex using deep brain stimulation.


Journal

Nature neuroscience
ISSN: 1546-1726
Titre abrégé: Nat Neurosci
Pays: United States
ID NLM: 9809671

Informations de publication

Date de publication:
22 Feb 2024
Historique:
received: 02 03 2023
accepted: 05 01 2024
medline: 23 2 2024
pubmed: 23 2 2024
entrez: 22 2 2024
Statut: aheadofprint

Résumé

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.

Identifiants

pubmed: 38388734
doi: 10.1038/s41593-024-01570-1
pii: 10.1038/s41593-024-01570-1
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : Project-ID 424778381 - TRR 295
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : Project-ID 424778381 - TRR 295
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : Project-ID 424778381 - TRR 295
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : Project-ID FI 2309/1-1
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : Project-ID FI 2309/2-1
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : Project-ID 424778381 - TRR 295
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : Project-ID 347325977
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : Project-ID 424778381 - TRR 2955
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : Project-ID 424778381 - TRR 295
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : Project-ID 431549029-C07 amp;#x2013; SFB 1451
Organisme : Deutsches Zentrum für Luft- und Raumfahrt (German Centre for Air and Space Travel)
ID : DynaSti grant within the EU Joint Programme Neurodegenerative Disease Research, JPND
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : R01 13478451
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : 2R01 MH113929
Organisme : U.S. Department of Health & Human Services | National Institutes of Health (NIH)
ID : the BRAIN Initiative CONNECTS comprehensive center award UM1-NS132358
Organisme : Einstein Stiftung Berlin (Einstein Foundation Berlin)
ID : PhD Scholarship (Einstein Center for Neurosciences)
Organisme : Einstein Stiftung Berlin (Einstein Foundation Berlin)
ID : PhD Scholarship (Einstein Center for Neurosciences)
Organisme : Einstein Stiftung Berlin (Einstein Foundation Berlin)
ID : PhD Scholarship (Einstein Center for Neurosciences Berlin)
Organisme : Agence Nationale de la Recherche (French National Research Agency)
ID : grant "Infrastructure d'Avenir en Biologie Santé - ANR-11-INBS-0006"
Organisme : Agence Nationale de la Recherche (French National Research Agency)
ID : grant ANR-CE17 "NeurOCD"
Organisme : RCUK | Medical Research Council (MRC)
ID : Grant No. MR/J012009/1
Organisme : RCUK | Medical Research Council (MRC)
ID : Grant No. MR/J012009/1

Informations de copyright

© 2024. The Author(s).

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Auteurs

Barbara Hollunder (B)

Movement Disorders and Neuromodulation Unit, Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany.
Einstein Center for Neurosciences Berlin, Charité - Universitätsmedizin Berlin, Berlin, Germany.
Berlin School of Mind and Brain, Humboldt-Universität zu Berlin, Berlin, Germany.

Jill L Ostrem (JL)

Movement Disorders and Neuromodulation Centre, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA.

Ilkem Aysu Sahin (IA)

Movement Disorders and Neuromodulation Unit, Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany.
Einstein Center for Neurosciences Berlin, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Nanditha Rajamani (N)

Movement Disorders and Neuromodulation Unit, Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Simón Oxenford (S)

Movement Disorders and Neuromodulation Unit, Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Konstantin Butenko (K)

Center for Brain Circuit Therapeutics, Department of Neurology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.

Clemens Neudorfer (C)

Center for Brain Circuit Therapeutics, Department of Neurology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
Department of Neurosurgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Pablo Reinhardt (P)

Department of Psychiatry and Psychotherapy, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Patricia Zvarova (P)

Movement Disorders and Neuromodulation Unit, Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany.
Einstein Center for Neurosciences Berlin, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Mircea Polosan (M)

Université Grenoble Alpes, Grenoble, France.
Inserm, U1216, Grenoble Institut des Neurosciences, Grenoble, France.
Department of Psychiatry, Centre Hospitalier Universitaire Grenoble Alpes, Grenoble, France.

Harith Akram (H)

Unit of Functional Neurosurgery, UCL Queen Square Institute of Neurology, London, UK.
Victor Horsley Department of Neurosurgery, The National Hospital for Neurology and Neurosurgery, London, UK.

Matteo Vissani (M)

Department of Neurosurgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.
The BioRobotics Institute, Scuola Superiore Sant'Anna, Pisa, Italy.
Department of Excellence in Robotics and AI, Scuola Superiore Sant'Anna, Pisa, Italy.

Chencheng Zhang (C)

Department of Neurosurgery, Rujin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.

Bomin Sun (B)

Department of Neurosurgery, Rujin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.

Pavel Navratil (P)

Department of Neurology, University Hospital Würzburg, Würzburg, Germany.

Martin M Reich (MM)

Department of Neurology, University Hospital Würzburg, Würzburg, Germany.

Jens Volkmann (J)

Department of Neurology, University Hospital Würzburg, Würzburg, Germany.

Fang-Cheng Yeh (FC)

Department of Neurological Surgery, University of Pittsburgh, Pittsburgh, PA, USA.

Juan Carlos Baldermann (JC)

Department of Psychiatry and Psychotherapy, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
Department of Neurology, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.

Till A Dembek (TA)

Center for Brain Circuit Therapeutics, Department of Neurology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.
Department of Neurology, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.

Veerle Visser-Vandewalle (V)

Department of Stereotactic and Functional Neurosurgery, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.

Eduardo Joaquim Lopes Alho (EJL)

Clinic of Pain and Functional Neurosurgery, São Paulo, Brazil.

Paulo Roberto Franceschini (PR)

Department of Neurology and Neurosurgery, University of Caxias do Sul, Rio Grande do Sul, Brazil.

Pranav Nanda (P)

Department of Neurosurgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Carsten Finke (C)

Einstein Center for Neurosciences Berlin, Charité - Universitätsmedizin Berlin, Berlin, Germany.
Berlin School of Mind and Brain, Humboldt-Universität zu Berlin, Berlin, Germany.
Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Andrea A Kühn (AA)

Movement Disorders and Neuromodulation Unit, Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany.
Einstein Center for Neurosciences Berlin, Charité - Universitätsmedizin Berlin, Berlin, Germany.
Berlin School of Mind and Brain, Humboldt-Universität zu Berlin, Berlin, Germany.
NeuroCure Cluster of Excellence, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Darin D Dougherty (DD)

Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

R Mark Richardson (RM)

Department of Neurosurgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Hagai Bergman (H)

Edmond and Lily Safra Center for Brain Sciences, The Hebrew University, Jerusalem, Israel.
Department of Medical Neurobiology, Institute of Medical Research Israel-Canada, The Hebrew University, Hadassah Medical School, Jerusalem, Israel.
Department of Neurosurgery, Hadassah Medical Center, Jerusalem, Israel.

Mahlon R DeLong (MR)

Department of Neurology, Emory University School of Medicine, Atlanta, GA, USA.

Alberto Mazzoni (A)

The BioRobotics Institute, Scuola Superiore Sant'Anna, Pisa, Italy.
Department of Excellence in Robotics and AI, Scuola Superiore Sant'Anna, Pisa, Italy.

Luigi M Romito (LM)

Parkinson and Movement Disorders Unit, Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan, Italy.

Himanshu Tyagi (H)

Unit of Functional Neurosurgery, UCL Queen Square Institute of Neurology, London, UK.
Department of Neuropsychiatry, The National Hospital for Neurology and Neurosurgery, London, UK.

Ludvic Zrinzo (L)

Unit of Functional Neurosurgery, UCL Queen Square Institute of Neurology, London, UK.
Victor Horsley Department of Neurosurgery, The National Hospital for Neurology and Neurosurgery, London, UK.

Eileen M Joyce (EM)

Unit of Functional Neurosurgery, UCL Queen Square Institute of Neurology, London, UK.
Department of Neuropsychiatry, The National Hospital for Neurology and Neurosurgery, London, UK.

Stephan Chabardes (S)

Université Grenoble Alpes, Grenoble, France.
Inserm, U1216, Grenoble Institut des Neurosciences, Grenoble, France.
Department of Neurosurgery, Centre Hospitalier Universitaire Grenoble Alpes, Grenoble, France.

Philip A Starr (PA)

Department of Neurological Surgery, University of California, San Francisco, San Francisco, CA, USA.

Ningfei Li (N)

Movement Disorders and Neuromodulation Unit, Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany. ningfei.li@gmail.com.

Andreas Horn (A)

Movement Disorders and Neuromodulation Unit, Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany. ahorn1@bwh.harvard.edu.
Einstein Center for Neurosciences Berlin, Charité - Universitätsmedizin Berlin, Berlin, Germany. ahorn1@bwh.harvard.edu.
Center for Brain Circuit Therapeutics, Department of Neurology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA. ahorn1@bwh.harvard.edu.
Department of Neurosurgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA. ahorn1@bwh.harvard.edu.

Classifications MeSH