Mapping Dysfunctional Circuits in the Frontal Cortex Using Deep Brain Stimulation.

Connectome Deep Brain Stimulation (DBS) Dystonia Obsessive-Compulsive Disorder (OCD) Parkinson’s disease (PD) Structural Connectivity Subthalamic Nucleus (STN) Tourette’s syndrome (TS)

Journal

medRxiv : the preprint server for health sciences
Titre abrégé: medRxiv
Pays: United States
ID NLM: 101767986

Informations de publication

Date de publication:
25 Aug 2023
Historique:
pubmed: 23 3 2023
medline: 23 3 2023
entrez: 22 3 2023
Statut: epublish

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)function remains largely elusive. Here, we study 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 segregate the frontal cortex into circuits that became dysfunctional in each of them. Dysfunctional circuits were topographically arranged from occipital to rostral, ranging from interconnections with sensorimotor cortices in dystonia, with 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 impairment in the human brain.

Identifiants

pubmed: 36945497
doi: 10.1101/2023.03.07.23286766
pmc: PMC10029043
pii:
doi:

Banques de données

Dryad
['10.5061/dryad.nzs7h44q2']

Types de publication

Preprint

Langues

eng

Subventions

Organisme : NIMH NIH HHS
ID : R01 MH130666
Pays : United States

Déclaration de conflit d'intérêts

Declaration of Competing Interests J.L.O. reports research grant support from Medtronic and Boston Scientific and is a consultant for Abbott, outside of the submitted work. M.M.R. reports grant support and honoraria for speaking from Medtronic and Boston Scientific, outside of the submitted work. J.V. reports grants and personal fees from Medtronic Inc., grants, and personal fees from Boston Scientific, personal fees from Abbott, outside of the submitted work. H.B. is consultant of Alpha-Omega, outside of the submitted work. S.C. is consultant for Medtronic and Boston Scientific, outside of the submitted work. A.H. is a consultant for FxNeuromodulation and Abbott, and reports lecture fees from Boston Scientific, outside of the submitted work. B.H., I.A.S., N.R., S.O., K.B., C.N., P.R., P.Z., M.P., H.A., M.V., C.Z., B.S., P.N., F.-C.Y., J.C.B., T.A.D., V.V.-V., E.J.L.A., P.R.F., C.F., A.A.K., P.N., D.D.D., R.M.R., M.R.D., A.M., L.M.R., H.T., L.Z., E.M.J., P.A.S., and N.L. report no competing interests.

Auteurs

Barbara Hollunder (B)

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)

Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany.
Einstein Center for Neurosciences Berlin, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Nanditha Rajamani (N)

Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Simón Oxenford (S)

Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Konstantin Butenko (K)

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

Clemens Neudorfer (C)

Center for Brain Circuit Therapeutics, Department of Neurology, Brigham & 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)

Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany.
Einstein Center for Neurosciences Berlin, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Mircea Polosan (M)

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

Harith Akram (H)

Department of Clinical and Movement Neurosciences, University College London Queen Square Institute of Neurology, London, UK.
National Hospital for Neurology and Neurosurgery, University College London Queen Square Institute of Neurology, 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)

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)

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.

Andrea A Kühn (AA)

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)

The 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, Hassadah 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)

Department of Clinical and Movement Neurosciences, University College London Queen Square Institute of Neurology, London, UK.
National Hospital for Neurology and Neurosurgery, University College London Queen Square Institute of Neurology, London, UK.

Ludvic Zrinzo (L)

Department of Clinical and Movement Neurosciences, University College London Queen Square Institute of Neurology, London, UK.
National Hospital for Neurology and Neurosurgery, University College London Queen Square Institute of Neurology, London, UK.

Eileen M Joyce (EM)

Department of Clinical and Movement Neurosciences, University College London Queen Square Institute of Neurology, London, UK.
National Hospital for Neurology and Neurosurgery, University College London Queen Square Institute of Neurology, London, UK.

Stephan Chabardes (S)

Univ. 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)

Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Andreas Horn (A)

Department of Neurology, Charité - Universitätsmedizin Berlin, Berlin, Germany.
Einstein Center for Neurosciences Berlin, Charité - Universitätsmedizin Berlin, Berlin, Germany.
Center for Brain Circuit Therapeutics, Department of Neurology, Brigham & Women's Hospital, Harvard Medical School, Boston, MA, USA.
Department of Neurosurgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Classifications MeSH