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Combining brain perturbation and neuroimaging in non-human primates

Klink, P. Christiaan and Aubry, Jean-François and Ferrera, Vincent P. and Fox, Andrew S. and Froudist-Walsh, Sean and Jarraya, Béchir and Konofagou, Elisa E. and Krauzlis, Richard J. and Messinger, Adam and Mitchell, Anna S. and Ortiz-Rios, Michael and Oya, Hiroyuki and Roberts, Angela C. and Roe, Anna Wang and Rushworth, Matthew F. S. and Sallet, Jérôme and Schmid, Michael Christoph and Schroeder, Charles E. and Tasserie, Jordy and Tsao, Doris Y. and Uhrig, Lynn and Vanduffel, Wim and Wilke, Melanie and Kagan, Igor and Petkov, Christopher I. (2021) Combining brain perturbation and neuroimaging in non-human primates. NeuroImage, 235 . Art. No. 118017. ISSN 1053-8119. doi:10.1016/j.neuroimage.2021.118017. https://resolver.caltech.edu/CaltechAUTHORS:20210406-080702298

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Abstract

Brain perturbation studies allow detailed causal inferences of behavioral and neural processes. Because the combination of brain perturbation methods and neural measurement techniques is inherently challenging, research in humans has predominantly focused on non-invasive, indirect brain perturbations, or neurological lesion studies. Non-human primates have been indispensable as a neurobiological system that is highly similar to humans while simultaneously being more experimentally tractable, allowing visualization of the functional and structural impact of systematic brain perturbation. This review considers the state of the art in non-human primate brain perturbation with a focus on approaches that can be combined with neuroimaging. We consider both non-reversible (lesions) and reversible or temporary perturbations such as electrical, pharmacological, optical, optogenetic, chemogenetic, pathway-selective, and ultrasound based interference methods. Method-specific considerations from the research and development community are offered to facilitate research in this field and support further innovations. We conclude by identifying novel avenues for further research and innovation and by highlighting the clinical translational potential of the methods.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.neuroimage.2021.118017DOIArticle
https://doi.org/10.31219/osf.io/z4x89DOIDiscussion Paper
ORCID:
AuthorORCID
Klink, P. Christiaan0000-0002-6784-7842
Aubry, Jean-François0000-0003-2644-3945
Ferrera, Vincent P.0000-0002-6599-7740
Fox, Andrew S.0000-0003-0695-3323
Froudist-Walsh, Sean0000-0003-4070-067X
Jarraya, Béchir0000-0003-0878-763X
Messinger, Adam0000-0002-8939-7897
Mitchell, Anna S.0000-0001-8996-1067
Ortiz-Rios, Michael0000-0003-4862-654X
Oya, Hiroyuki0000-0002-1733-5478
Roe, Anna Wang0000-0003-4146-9705
Sallet, Jérôme0000-0002-7878-0209
Schmid, Michael Christoph0000-0003-1424-130X
Tsao, Doris Y.0000-0003-1083-1919
Uhrig, Lynn0000-0002-2737-0197
Kagan, Igor0000-0002-1814-4200
Petkov, Christopher I.0000-0002-4932-7907
Additional Information:© 2021 The Author(s). Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). Received 11 September 2020, Revised 7 March 2021, Accepted 22 March 2021, Available online 29 March 2021. This work was supported by NIH-MH112142 (V.F. and E.K.); California National Primate Research Center Base Grant (P51-OD011107) (A.F.); Fondation Bettencourt Schueller, France and Human Brain Project (B.J., L.U., J.T.); the Intramural Research Program of the NIMH (ZIA MH002918) (A.M.); Wellcome Trust (WT 110157/Z/15/Z) (A.S.M.); European Research Council (ERC StG, OptoVision, 637638) (M.C.S and M.O.R.); National Key R&D Program of China 2018YFA0701400 (A.W.R.); Chinese NSF (81430010 and 31627802) (A.W.R.); Zhejiang province 2020C03004 (A.W.R.); Chinese National R&D Program Grant 2015AA020515 (A.W.R.); IDEXLYON “IMPULSION 2020 grant (IDEX/IMP/2020/14) (J.S.); Howard Hughes Medical Institute (D.T.); KU Leuven grant C14/17/109 (W.V.); the National Eye Institute Intramural Research Program (ZIA EY000511) at the National Institutes of Health, U.S.A. (W.V.); Fonds Wetenschappelijk Onderzoek-Vlaanderen (FWO) G0D5817N, G0B8617N, G0C1920N, G0E0520N, VS02219N (W.V.); the European Union's Horizon 2020 Framework Programme for Research and Innovation under Grant Agreement No 945539 (Human Brain Project SGA3) (W.V.); Hermann and Lilly Schilling Foundation; German Research Foundation (DFG) grants WI 4046/1-1 and Research Unit GA1475-B4, KA 3726/2-1, Primate Platform of DFG Center for Nanoscale Microscopy & Molecular Physiology of the Brain (CNMPB) (M.W. and I.K.); Wellcome Trust (WT092606AIA) (C.I.P.); European Research Council Horizon 2020 (ERC CoG, MECHIDENT 724198) (C.I.P.); the Bettencourt Schueller Foundation (Ultrabrain project) (J.-F. A.); the French National Agency for Research (ANR-10-EQPX-15) (J.-F. A.):and the National Institutes of Health (with Matthew Howard III: R01-DC04290) (C.I.P.); All research discussed in this work was performed in accordance with institutional and nationally approved oversight, such as the NIH Guide for Care and Use of Laboratory Animals, the U.K. Animals (Scientific Procedures) Act, 1986, and European Directive 2010/63/EU. This paper does not contain original data or analysis. The authors declare no competing financial interests.
Funders:
Funding AgencyGrant Number
NIHMH112142
NIHP51-OD011107
Fondation Bettencourt SchuellerUNSPECIFIED
Human Brain ProjectUNSPECIFIED
NIHMH002918
Wellcome Trust110157/Z/15/Z
European Research Council (ERC)637638
National Key Research and Development Program of China2018YFA0701400
National Natural Science Foundation of China81430010
National Natural Science Foundation of China31627802
Zhejiang Province2020C03004
Ministry of Science and Technology (Taipei)2015AA020515
IDEXLYONIDEX/IMP/2020/14
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Katholieke Universiteit LeuvenC14/17/109
National Eye InstituteEY000511
Fonds Wetenschappelijk Onderzoek (FWO)G0D5817N
Fonds Wetenschappelijk Onderzoek (FWO)G0B8617N
Fonds Wetenschappelijk Onderzoek (FWO)G0C1920N
Fonds Wetenschappelijk Onderzoek (FWO)G0E0520N
Fonds Wetenschappelijk Onderzoek (FWO)VS02219N
European Research Council (ERC)945539
Hermann and Lilly Schilling FoundationUNSPECIFIED
Deutsche Forschungsgemeinschaft (DFG)WI 4046/1-1
Deutsche Forschungsgemeinschaft (DFG)GA1475-B4
Deutsche Forschungsgemeinschaft (DFG)KA 3726/2-1
Wellcome TrustWT092606AIA
European Research Council (ERC)724198
Bettencourt Schueller FoundationUNSPECIFIED
Agence Nationale pour la Recherche (ANR)ANR-10-EQPX-15
NIHR01-DC04290
Subject Keywords:Microstimulation; Optogenetics; Chemogenetics; Ultrasound; Lesion; Infrared; Causality; fMRI; primates
DOI:10.1016/j.neuroimage.2021.118017
Record Number:CaltechAUTHORS:20210406-080702298
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210406-080702298
Official Citation:P. Christiaan Klink, Jean-François Aubry, Vincent P. Ferrera, Andrew S. Fox, Sean Froudist-Walsh, Béchir Jarraya, Elisa E. Konofagou, Richard J. Krauzlis, Adam Messinger, Anna S. Mitchell, Michael Ortiz-Rios, Hiroyuki Oya, Angela C. Roberts, Anna Wang Roe, Matthew F.S. Rushworth, Jérôme Sallet, Michael Christoph Schmid, Charles E. Schroeder, Jordy Tasserie, Doris Y. Tsao, Lynn Uhrig, Wim Vanduffel, Melanie Wilke, Igor Kagan, Christopher I. Petkov, Combining brain perturbation and neuroimaging in non-human primates, NeuroImage, Volume 235, 2021, 118017, ISSN 1053-8119, https://doi.org/10.1016/j.neuroimage.2021.118017.
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:108627
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:07 Apr 2021 23:36
Last Modified:23 Apr 2021 17:59

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