Optimal deep brain stimulation sites and networks for stimulation of the fornix in Alzheimer's disease.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
14 12 2022
Historique:
received: 05 11 2021
accepted: 27 10 2022
entrez: 14 12 2022
pubmed: 15 12 2022
medline: 17 12 2022
Statut: epublish

Résumé

Deep brain stimulation (DBS) to the fornix is an investigational treatment for patients with mild Alzheimer's Disease. Outcomes from randomized clinical trials have shown that cognitive function improved in some patients but deteriorated in others. This could be explained by variance in electrode placement leading to differential engagement of neural circuits. To investigate this, we performed a post-hoc analysis on a multi-center cohort of 46 patients with DBS to the fornix (NCT00658125, NCT01608061). Using normative structural and functional connectivity data, we found that stimulation of the circuit of Papez and stria terminalis robustly associated with cognitive improvement (R = 0.53, p < 0.001). On a local level, the optimal stimulation site resided at the direct interface between these structures (R = 0.48, p < 0.001). Finally, modulating specific distributed brain networks related to memory accounted for optimal outcomes (R = 0.48, p < 0.001). Findings were robust to multiple cross-validation designs and may define an optimal network target that could refine DBS surgery and programming.

Identifiants

pubmed: 36517479
doi: 10.1038/s41467-022-34510-3
pii: 10.1038/s41467-022-34510-3
pmc: PMC9751139
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

7707

Subventions

Organisme : NIA NIH HHS
ID : P30 AG072979
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH130666
Pays : United States

Informations de copyright

© 2022. The Author(s).

Références

Ann Neurol. 2020 Jun;87(6):962-975
pubmed: 32239535
Neuroimage. 2015 Aug 15;117:267-83
pubmed: 25998957
JAMA Neurol. 2013 Nov;70(11):1389-95
pubmed: 24018960
Sci Data. 2015 Jul 07;2:150031
pubmed: 26175908
Neuromodulation. 2018 Feb;21(2):184-190
pubmed: 28653404
Trends Cogn Sci. 2010 Nov;14(11):489-96
pubmed: 20884276
BMC Med Ethics. 2018 Jun 11;19(1):41
pubmed: 29886845
Nature. 2016 Dec 7;540(7632):230-235
pubmed: 27929004
Acta Neuropathol. 1991;82(4):239-59
pubmed: 1759558
J Comp Neurol. 1997 Jul 28;384(2):312-20
pubmed: 9215725
Neurosci Biobehav Rev. 2013 Jun;37(5):753-65
pubmed: 23523750
Front Aging Neurosci. 2014 Sep 11;6:241
pubmed: 25309426
Elife. 2022 May 20;11:
pubmed: 35594135
Ann Neurol. 2017 Jul;82(1):67-78
pubmed: 28586141
J Alzheimers Dis. 2018;64(2):597-606
pubmed: 29914028
Alzheimer Dis Assoc Disord. 1997;11 Suppl 2:S13-21
pubmed: 9236948
Ann Neurol. 2010 Oct;68(4):521-34
pubmed: 20687206
Brain. 2019 Oct 1;142(10):3086-3098
pubmed: 31377766
Brain. 2021 Oct 22;144(9):2837-2851
pubmed: 33905474
Brain Stimul. 2021 May-Jun;14(3):549-563
pubmed: 33757931
PLoS Comput Biol. 2017 Oct 23;13(10):e1005649
pubmed: 29059185
Ann Neurol. 2008 Jan;63(1):119-23
pubmed: 18232017
Alzheimers Dement. 2011 May;7(3):257-62
pubmed: 21514247
Nature. 2016 Nov 09;539(7628):187-196
pubmed: 27830780
Trends Cogn Sci. 2006 Feb;10(2):59-63
pubmed: 16406760
Neuroimage. 2021 Jan 1;224:117307
pubmed: 32861787
Am J Manag Care. 2020 Aug;26(8 Suppl):S177-S183
pubmed: 32840331
Biol Psychiatry. 2019 May 1;85(9):735-743
pubmed: 30777287
Neuromodulation. 2021 Feb;24(2):248-258
pubmed: 33389779
Ann Clin Transl Neurol. 2015 Apr;2(4):427-32
pubmed: 25909087
Science. 2020 Aug 21;369(6506):988-992
pubmed: 32732281
Neuroimage. 2020 Oct 1;219:117018
pubmed: 32505698
Brain Res. 2013 Jun 17;1515:12-8
pubmed: 23583480
Surg Neurol Int. 2018 Mar 07;9:58
pubmed: 29576909
Brain. 2014 Jan;137(Pt 1):109-21
pubmed: 24277721
Biomed Eng Online. 2018 Mar 27;17(1):37
pubmed: 29580236
Sci Data. 2021 Apr 29;8(1):122
pubmed: 33927203
J Alzheimers Dis. 2018;62(2):621-633
pubmed: 29400666
Neuron. 2013 Feb 6;77(3):406-24
pubmed: 23395370
J Alzheimers Dis. 2015;46(2):351-64
pubmed: 25737041
Brain. 2016 Jul;139(Pt 7):1877-90
pubmed: 27190025
IEEE Trans Biomed Eng. 2015 Feb;62(2):664-672
pubmed: 25350910
J Neurosurg. 2016 Jul;125(1):75-84
pubmed: 26684775
Neuron. 2011 Dec 8;72(5):692-7
pubmed: 22153367
Nat Commun. 2020 Jul 3;11(1):3364
pubmed: 32620886
IEEE Trans Med Imaging. 2010 Sep;29(9):1626-35
pubmed: 20304721
Proc Natl Acad Sci U S A. 2022 Apr 5;119(14):e2114985119
pubmed: 35357970
Biol Psychiatry. 2021 Nov 15;90(10):678-688
pubmed: 34482949
Am J Psychiatry. 1984 Nov;141(11):1356-64
pubmed: 6496779
IEEE Trans Med Imaging. 2009 Jul;28(7):1023-36
pubmed: 19150781
Neuropsychologia. 2009 Sep;47(11):2314-29
pubmed: 19524095
Science. 2006 Mar 3;311(5765):1290-3
pubmed: 16513983
Front Aging Neurosci. 2015 Jan 21;7:1
pubmed: 25653617
Curr Opin Neurol. 2019 Aug;32(4):511-520
pubmed: 30844863
PLoS One. 2017 Apr 25;12(4):e0176132
pubmed: 28441410
Sci Data. 2019 Oct 30;6(1):244
pubmed: 31666530
Clin Neurophysiol. 2004 Jul;115(7):1490-505
pubmed: 15203050
Med Image Anal. 2008 Feb;12(1):26-41
pubmed: 17659998
Neuroinformatics. 2011 Dec;9(4):371-80
pubmed: 21360205
Biol Psychiatry. 2021 Nov 15;90(10):701-713
pubmed: 34134839
J Alzheimers Dis. 2016 Sep 6;54(2):777-87
pubmed: 27567810
Brain. 1963 Dec;86:595-696
pubmed: 14090522
Neuroimage. 2018 Apr 15;170:132-150
pubmed: 27765611
Int J Alzheimers Dis. 2011;2011:535816
pubmed: 21760988
Neuroimage. 2009 Jul 1;46(3):786-802
pubmed: 19195496
Cell. 2019 Apr 4;177(2):256-271.e22
pubmed: 30879788
JAMA Neurol. 2015 Nov;72(11):1252-60
pubmed: 26408865
Alzheimers Dement. 2012 Jan;8(1):1-13
pubmed: 22265587
Sci Data. 2020 Sep 15;7(1):305
pubmed: 32934244
Neuroimage Clin. 2017 Oct 06;17:80-89
pubmed: 29062684
Brain. 2010 Nov;133(11):3301-14
pubmed: 20688814
JAMA Psychiatry. 2020 May 1;77(5):534-540
pubmed: 31774490
Proc Natl Acad Sci U S A. 2004 Mar 30;101(13):4637-42
pubmed: 15070770
Neuroimage. 2015 Feb 15;107:127-135
pubmed: 25498389
Neurosci Biobehav Rev. 2017 Jul;78:161-177
pubmed: 28445741
N Engl J Med. 2019 Aug 22;381(8):783-785
pubmed: 31433930
J Neurophysiol. 2011 Sep;106(3):1125-65
pubmed: 21653723
Alzheimers Dement. 2021 May;17(5):777-787
pubmed: 33480187
Neurology. 2002 Jun 25;58(12):1791-800
pubmed: 12084879
Neuroimage. 2019 Jan 1;184:293-316
pubmed: 30179717
Neuroimage. 2017 Apr 15;150:395-404
pubmed: 28163141
Alzheimers Dement. 2012;8(2):105-13
pubmed: 22404852
Neuromodulation. 2022 Aug;25(6):877-887
pubmed: 33476474

Auteurs

Ana Sofía Ríos (AS)

Movement Disorder and Neuromodulation Unit, Department of Neurology, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.

Simón Oxenford (S)

Movement Disorder and Neuromodulation Unit, Department of Neurology, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.

Clemens Neudorfer (C)

Movement Disorder and Neuromodulation Unit, Department of Neurology, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.

Konstantin Butenko (K)

Movement Disorder and Neuromodulation Unit, Department of Neurology, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.

Ningfei Li (N)

Movement Disorder and Neuromodulation Unit, Department of Neurology, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.

Nanditha Rajamani (N)

Movement Disorder and Neuromodulation Unit, Department of Neurology, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.

Alexandre Boutet (A)

Division of Neurosurgery, Department of Surgery, University Health Network and University of Toronto, Toronto, ON, M5T2S8, Canada.
Krembil Research Institute, University of Toronto, Toronto, ON, M5T2S8, Canada.
Joint Department of Medical Imaging, University of Toronto, Toronto, ON, M5T1W7, Canada.

Gavin J B Elias (GJB)

Division of Neurosurgery, Department of Surgery, University Health Network and University of Toronto, Toronto, ON, M5T2S8, Canada.
Krembil Research Institute, University of Toronto, Toronto, ON, M5T2S8, Canada.

Jurgen Germann (J)

Division of Neurosurgery, Department of Surgery, University Health Network and University of Toronto, Toronto, ON, M5T2S8, Canada.
Krembil Research Institute, University of Toronto, Toronto, ON, M5T2S8, Canada.

Aaron Loh (A)

Division of Neurosurgery, Department of Surgery, University Health Network and University of Toronto, Toronto, ON, M5T2S8, Canada.
Krembil Research Institute, University of Toronto, Toronto, ON, M5T2S8, Canada.

Wissam Deeb (W)

UMass Chan Medical School, Department of Neurology, Worcester, MA, 01655, USA.
UMass Memorial Health, Department of Neurology, Worcester, MA, 01655, USA.

Fuyixue Wang (F)

Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Harvard Medical School, Massachusetts General Hospital, Charlestown, MA, USA.
Harvard-MIT Health Sciences and Technology, MIT, Cambridge, MA, USA.

Kawin Setsompop (K)

Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Harvard Medical School, Massachusetts General Hospital, Charlestown, MA, USA.
Harvard-MIT Health Sciences and Technology, MIT, Cambridge, MA, USA.
Department of Radiology, Stanford University, Stanford, CA, USA.

Bryan Salvato (B)

University of Florida Health Jacksonville, Jacksonville, FL, USA.

Leonardo Brito de Almeida (LB)

Norman Fixel Institute for Neurological Diseases, Departments of Neurology and Neurosurgery, University of Florida, Gainesville, FL, USA.

Kelly D Foote (KD)

Norman Fixel Institute for Neurological Diseases, Departments of Neurology and Neurosurgery, University of Florida, Gainesville, FL, USA.

Robert Amaral (R)

Cerebral Imaging Centre, Douglas Research Centre, Montreal, QC, Canada.

Paul B Rosenberg (PB)

Department of Psychiatry and Behavioral Sciences and Richman Family Precision Medicine Center of Excellence, School of Medicine, Johns Hopkins University, Baltimore, MD, USA.

David F Tang-Wai (DF)

Krembil Research Institute, University of Toronto, Toronto, ON, M5T2S8, Canada.
Department of Medicine, Division of Neurology, University Health Network and University of Toronto, Toronto, ON, M5T2S8, Canada.

David A Wolk (DA)

Department of Neurology, University of Pennsylvania, Philadelphia, PA, USA.

Anna D Burke (AD)

Barrow Neurological Institute, Phoenix, AZ, USA.

Stephen Salloway (S)

Department of Psychiatry and Human Behavior and Neurology, Alpert Medical School of Brown University, Providence, RI, USA.
Memory & Aging Program, Butler Hospital, Providence, USA.

Marwan N Sabbagh (MN)

Barrow Neurological Institute, Phoenix, AZ, USA.

M Mallar Chakravarty (MM)

Cerebral Imaging Centre, Douglas Research Centre, Montreal, QC, Canada.
Department of Psychiatry, McGill University, Montreal, QC, Canada.
Biological and Biomedical Engineering, McGill University, Montreal, QC, Canada.

Gwenn S Smith (GS)

Department of Psychiatry and Behavioral Sciences and Richman Family Precision Medicine Center of Excellence, School of Medicine, Johns Hopkins University, Baltimore, MD, USA.

Constantine G Lyketsos (CG)

Department of Psychiatry and Behavioral Sciences and Richman Family Precision Medicine Center of Excellence, School of Medicine, Johns Hopkins University, Baltimore, MD, USA.

Michael S Okun (MS)

Norman Fixel Institute for Neurological Diseases, Departments of Neurology and Neurosurgery, University of Florida, Gainesville, FL, USA.

William S Anderson (WS)

Johns Hopkins School of Medicine, Baltimore, MD, USA.

Zoltan Mari (Z)

Johns Hopkins School of Medicine, Baltimore, MD, USA.
Cleveland Clinic Lou Ruvo Center for Brain Health, Las Vegas, NV, USA.

Francisco A Ponce (FA)

Barrow Neurological Institute, Phoenix, AZ, USA.

Andres M Lozano (AM)

Division of Neurosurgery, Department of Surgery, University Health Network and University of Toronto, Toronto, ON, M5T2S8, Canada.
Krembil Research Institute, University of Toronto, Toronto, ON, M5T2S8, Canada.

Andreas Horn (A)

Movement Disorder and Neuromodulation Unit, Department of Neurology, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany. ahorn1@bwh.harvard.edu.
Center for Brain Circuit Therapeutics, Department of Neurology, Brigham and Women's Hospital, Boston, MA, USA. ahorn1@bwh.harvard.edu.
Departments of Neurology and Neurosurgery, Massachusetts General Hospital, Boston, MA, USA. ahorn1@bwh.harvard.edu.

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