An Open Resource for Non-human Primate Optogenetics

Sébastien Tremblay; Leah Acker; Arash Afraz; Daniel L. Albaugh; Hidetoshi Amita; Ariana R. Andrei; Alessandra Angelucci; Amir Aschner; Puiu F. Balan; Michele A. Basso; Giacomo Benvenuti; Martin O. Bohlen; Michael J. Caiola; Roberto Calcedo; James Cavanaugh; Yuzhi Chen; Spencer Chen; Mykyta M. Chernov; Andrew M. Clark; Ji Dai; Samantha R. Debes; Karl Deisseroth; Robert Desimone; Valentin Dragoi; Seth W. Egger; Mark A.G. Eldridge; Hala G. El-Nahal; Francesco Fabbrini; Frederick Federer; Christopher R. Fetsch; Michal G. Fortuna; Robert M. Friedman; Naotaka Fujii; Alexander Gail; Adriana Galvan; Supriya Ghosh; Marc Alwin Gieselmann; Roberto A. Gulli; Okihide Hikosaka; Eghbal A. Hosseini; Xing Hu; Janina Hüer; Ken ichi Inoue; Roger Janz; Mehrdad Jazayeri; Rundong Jiang; Niansheng Ju; Kohitij Kar; Carsten Klein; Adam Kohn; Misako Komatsu; Kazutaka Maeda; Julio C. Martinez-Trujillo; Masayuki Matsumoto; John H.R. Maunsell; Diego Mendoza-Halliday; Ilya E. Monosov; Ross S. Muers; Lauri Nurminen; Michael Ortiz-Rios; Daniel J. O'Shea; Stéphane Palfi; Christopher I. Petkov; Sorin Pojoga; Rishi Rajalingham; Charu Ramakrishnan; Evan D. Remington; Cambria Revsine; Anna W. Roe; Philip N. Sabes; Richard C. Saunders; Hansjörg Scherberger; Michael C. Schmid; Wolfram Schultz; Eyal Seidemann; Yann Suhan Senova; Michael N. Shadlen; David L. Sheinberg; Caitlin Siu; Yoland Smith; Selina S. Solomon; Marc A. Sommer; John L. Spudich; William R. Stauffer; Masahiko Takada; Shiming Tang; Alexander Thiele; Stefan Treue; Wim Vanduffel; Rufin Vogels; Matthew P. Whitmire; Thomas Wichmann; Robert H. Wurtz; Haoran Xu; Azadeh Yazdan-Shahmorad; Krishna V. Shenoy; James J. DiCarlo; Michael L. Platt

doi:10.1016/j.neuron.2020.09.027

An Open Resource for Non-human Primate Optogenetics

Sébastien Tremblay, Leah Acker, Arash Afraz, Daniel L. Albaugh, Hidetoshi Amita, Ariana R. Andrei, Alessandra Angelucci, Amir Aschner, Puiu F. Balan, Michele A. Basso, Giacomo Benvenuti, Martin O. Bohlen, Michael J. Caiola, Roberto Calcedo, James Cavanaugh, Yuzhi Chen, Spencer Chen, Mykyta M. Chernov, Andrew M. Clark, Ji DaiSamantha R. Debes, Karl Deisseroth, Robert Desimone, Valentin Dragoi, Seth W. Egger, Mark A.G. Eldridge, Hala G. El-Nahal, Francesco Fabbrini, Frederick Federer, Christopher R. Fetsch, Michal G. Fortuna, Robert M. Friedman, Naotaka Fujii, Alexander Gail, Adriana Galvan, Supriya Ghosh, Marc Alwin Gieselmann, Roberto A. Gulli, Okihide Hikosaka, Eghbal A. Hosseini, Xing Hu, Janina Hüer, Ken ichi Inoue, Roger Janz, Mehrdad Jazayeri, Rundong Jiang, Niansheng Ju, Kohitij Kar, Carsten Klein, Adam Kohn, Misako Komatsu, Kazutaka Maeda, Julio C. Martinez-Trujillo, Masayuki Matsumoto, John H.R. Maunsell, Diego Mendoza-Halliday, Ilya E. Monosov, Ross S. Muers, Lauri Nurminen, Michael Ortiz-Rios, Daniel J. O'Shea, Stéphane Palfi, Christopher I. Petkov, Sorin Pojoga, Rishi Rajalingham, Charu Ramakrishnan, Evan D. Remington, Cambria Revsine, Anna W. Roe, Philip N. Sabes, Richard C. Saunders, Hansjörg Scherberger, Michael C. Schmid, Wolfram Schultz, Eyal Seidemann, Yann Suhan Senova, Michael N. Shadlen, David L. Sheinberg, Caitlin Siu, Yoland Smith, Selina S. Solomon, Marc A. Sommer, John L. Spudich, William R. Stauffer, Masahiko Takada, Shiming Tang, Alexander Thiele, Stefan Treue, Wim Vanduffel, Rufin Vogels, Matthew P. Whitmire, Thomas Wichmann, Robert H. Wurtz, Haoran Xu, Azadeh Yazdan-Shahmorad, Krishna V. Shenoy, James J. DiCarlo, Michael L. Platt

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

33 Scopus citations

Abstract

Optogenetics has revolutionized neuroscience in small laboratory animals, but its effect on animal models more closely related to humans, such as non-human primates (NHPs), has been mixed. To make evidence-based decisions in primate optogenetics, the scientific community would benefit from a centralized database listing all attempts, successful and unsuccessful, of using optogenetics in the primate brain. We contacted members of the community to ask for their contributions to an open science initiative. As of this writing, 45 laboratories around the world contributed more than 1,000 injection experiments, including precise details regarding their methods and outcomes. Of those entries, more than half had not been published. The resource is free for everyone to consult and contribute to on the Open Science Framework website. Here we review some of the insights from this initial release of the database and discuss methodological considerations to improve the success of optogenetic experiments in NHPs.

Original language	English
Pages (from-to)	1075-1090.e6
Journal	Neuron
Volume	108
Issue number	6
DOIs	https://doi.org/10.1016/j.neuron.2020.09.027
State	Published - Dec 23 2020

Keywords

Gene therapy
Monkey
Monkeys
Non-human primates
Nonhuman primates
Open Science
Optical control
Optogenetic
Optogenetics
Viral vectors

Access to Document

10.1016/j.neuron.2020.09.027

Cite this

Tremblay, S., Acker, L., Afraz, A., Albaugh, D. L., Amita, H., Andrei, A. R., Angelucci, A., Aschner, A., Balan, P. F., Basso, M. A., Benvenuti, G., Bohlen, M. O., Caiola, M. J., Calcedo, R., Cavanaugh, J., Chen, Y., Chen, S., Chernov, M. M., Clark, A. M., ... Platt, M. L. (2020). An Open Resource for Non-human Primate Optogenetics. Neuron, 108(6), 1075-1090.e6. https://doi.org/10.1016/j.neuron.2020.09.027

@article{becbf5b0198b4aa8a811b1f5c704e479,

title = "An Open Resource for Non-human Primate Optogenetics",

abstract = "Optogenetics has revolutionized neuroscience in small laboratory animals, but its effect on animal models more closely related to humans, such as non-human primates (NHPs), has been mixed. To make evidence-based decisions in primate optogenetics, the scientific community would benefit from a centralized database listing all attempts, successful and unsuccessful, of using optogenetics in the primate brain. We contacted members of the community to ask for their contributions to an open science initiative. As of this writing, 45 laboratories around the world contributed more than 1,000 injection experiments, including precise details regarding their methods and outcomes. Of those entries, more than half had not been published. The resource is free for everyone to consult and contribute to on the Open Science Framework website. Here we review some of the insights from this initial release of the database and discuss methodological considerations to improve the success of optogenetic experiments in NHPs.",

keywords = "Gene therapy, Monkey, Monkeys, Non-human primates, Nonhuman primates, Open Science, Optical control, Optogenetic, Optogenetics, Viral vectors",

author = "S{\'e}bastien Tremblay and Leah Acker and Arash Afraz and Albaugh, {Daniel L.} and Hidetoshi Amita and Andrei, {Ariana R.} and Alessandra Angelucci and Amir Aschner and Balan, {Puiu F.} and Basso, {Michele A.} and Giacomo Benvenuti and Bohlen, {Martin O.} and Caiola, {Michael J.} and Roberto Calcedo and James Cavanaugh and Yuzhi Chen and Spencer Chen and Chernov, {Mykyta M.} and Clark, {Andrew M.} and Ji Dai and Debes, {Samantha R.} and Karl Deisseroth and Robert Desimone and Valentin Dragoi and Egger, {Seth W.} and Eldridge, {Mark A.G.} and El-Nahal, {Hala G.} and Francesco Fabbrini and Frederick Federer and Fetsch, {Christopher R.} and Fortuna, {Michal G.} and Friedman, {Robert M.} and Naotaka Fujii and Alexander Gail and Adriana Galvan and Supriya Ghosh and Gieselmann, {Marc Alwin} and Gulli, {Roberto A.} and Okihide Hikosaka and Hosseini, {Eghbal A.} and Xing Hu and Janina H{\"u}er and Inoue, {Ken ichi} and Roger Janz and Mehrdad Jazayeri and Rundong Jiang and Niansheng Ju and Kohitij Kar and Carsten Klein and Adam Kohn and Misako Komatsu and Kazutaka Maeda and Martinez-Trujillo, {Julio C.} and Masayuki Matsumoto and Maunsell, {John H.R.} and Diego Mendoza-Halliday and Monosov, {Ilya E.} and Muers, {Ross S.} and Lauri Nurminen and Michael Ortiz-Rios and O'Shea, {Daniel J.} and St{\'e}phane Palfi and Petkov, {Christopher I.} and Sorin Pojoga and Rishi Rajalingham and Charu Ramakrishnan and Remington, {Evan D.} and Cambria Revsine and Roe, {Anna W.} and Sabes, {Philip N.} and Saunders, {Richard C.} and Hansj{\"o}rg Scherberger and Schmid, {Michael C.} and Wolfram Schultz and Eyal Seidemann and Senova, {Yann Suhan} and Shadlen, {Michael N.} and Sheinberg, {David L.} and Caitlin Siu and Yoland Smith and Solomon, {Selina S.} and Sommer, {Marc A.} and Spudich, {John L.} and Stauffer, {William R.} and Masahiko Takada and Shiming Tang and Alexander Thiele and Stefan Treue and Wim Vanduffel and Rufin Vogels and Whitmire, {Matthew P.} and Thomas Wichmann and Wurtz, {Robert H.} and Haoran Xu and Azadeh Yazdan-Shahmorad and Shenoy, {Krishna V.} and DiCarlo, {James J.} and Platt, {Michael L.}",

note = "Funding Information: This manuscript was inspired by the PRIME-DE NeuroResource authored by Milham et al. (2018). We would like to thank the Jazayeri lab for the initial impetus for this collaboration and the MIT group (DiCarlo, Desimone, and Jazayeri labs) for providing the first in-house database of optogenetics experiments in NHPs that was used as a backbone for the current initiative. We are grateful to the Open Science Framework for hosting the database. Primary support for the work by M.L.P. and S. Tremblay is provided by the Charles E. Kaufman Foundation and the Canada Banting Fellowship. Primary support for A. Angelucci's lab is provided by the NIH (R01 EY026812, R01 EY019743, and BRAIN U01 NS099702) and the NSF (IOS 1755431). Support for L.N. is additionally provided by an NIH K99 grant (EY029374). Support for the work by A. Afraz (in part) came from the Intramural Research Program of the NIMH (ZIAMH002958). Support for the work contributed by M.A.B. was provided by NIH R01 EY013962 and R21 EY024516. R.D. acknowledges funding from NIH grant R01EY029666. Primary support for the work by J.D. is provided by the National Natural Science Foundation of China (31600870), the Youth Innovation Promotion Association CAS (2017120), and the Chinese Academy of Sciences International Partnership Program (172644KYSB20170004). Primary support for the work by D.L.S. and J.D. is provided by Defense Advanced Research Projects Agency (DARPA) Biological Technology Office (BTO) “REPAIR{\textquoteright}{\textquoteright} award N66001-10-C-2010 and NIH-EY014681. Support for the work by the Dragoi/Janz/Spudich labs is provided by the BRAIN Initiative (1U01MH109146 to V.D. R. Janz, and J.L.S.). Primary support for the work by N.F. and M.K. is provided by Brain/MINDS (JP19dm0207001) and KAKENHI (17H06034). Support for the work by the Treue, Gail, and Scherberger labs was provided by the Leibniz Association (WGL SAW-2014-DPZ-1) and the German Research Foundation (FOR 1847). Support for the work by D.L.A. M.J.C. X.H. A. Galvan, Y.S. and T.W. at Emory University is provided by NIH/NINDS (P50 NS098685 [Udall Center grant]) and a grant from NIH/ORIP to the Yerkes Center (P51 OD011132). Primary support for the work by H.A. K.M. and O.H. is provided by the National Eye Institute (project 1ZIAEY000415-16). Primary support for the work by E.D.R. S.W.E. E.H. and M.J. is provided by the National Institutes of Health (NINDS-NS078127). Primary support for the work by A. Aschner. A.K. and S.S.S. was provided by the NIH (EY026240), Fight for Sight, and the Stavros Niarchos Foundation/Research to Prevent Blindness. Primary support for the work by S.G. and J.H.R.M. is provided by NIH R01EY005911. Primary support for the work by S. Palfi and S.S. is provided by Fondation de France, Oxford Biomedica (Oxford, UK), and ARSC (France). Primary support for the work by R.S.M. and C.I.P. is provided by a Wellcome Trust Investigator Award, European Research Council Consolidator Award (MECHIDENT), and NIH NIDCD R01 (with M. Howard at the University of Iowa). Development of this technique was supported by NIH EY022853 to A.W.R. and Gene Stoner. Primary support for the work by C.K. M.O.-R. and M.C.S. is provided by DFG Emmy Noether grant SCHM 2806/1-1 and European Research Council grant OptoVision 637638. This work was supported by the Wellcome Trust (095495), European Research Council (293549), and NIH Caltech Conte Center (P50MH094258). Primary support for the work by the E.S. lab is provided by NIH-BRAIN U01NS099720, NEI R01EY016454, and DARPA-NESD-N66001-17-C-4012. Primary support for the work by C.R.F. and M.N.S. was provided by the Howard Hughes Medical Institute and the National Eye Institute (R01 EY11378). Primary support for the work by D.J.O. K.D. and K.V.S. is provided by an NSF Graduate Research Fellowship, Dr. Regina Casper Stanford Graduate Fellowship, Defense Advanced Research Projects Agency (DARPA) Biological Technology Office (BTO) “REPAIR{\textquoteright}{\textquoteright} award N66001-10-C-2010 (to K.V.S. and K.D.), DARPA BTO “NeuroFAST{\textquoteright}{\textquoteright} award W911NF-14-2-0013 (to K.D. and K.V.S.), Simons Foundation Collaboration on the Global Brain awards 325380 and 543045 (to K.V.S.), NIH Director's Pioneer Award 8DP1HD075623 (to K.V.S.), and the Howard Hughes Medical Institute (to K.D. and K.V.S.). Primary support for the work of K.I. M.M. and M.T. was provided by the Ministry of Education, Science, Sports, Culture, and Technology of Japan, the Japan Science and Technology Agency, and the Japan Agency for Medical Research and Development. Primary support for the work by N.J. R. Jiang, and S. Tang is provided by the National Natural Science Foundation of China and the National Basic Research Program of China. Primary support for the work by M.A.G. and A.T. is provided by the Medical Research Council. Primary support for the work by W.V. and P.F.B. is provided by the Research Foundation Flanders (FWO-Flanders), internal KU Leuven funds (C14/17/109), and the European Union Horizon 2020 Framework Program for Research and Innovation under grant agreement 785907. Primary support for the work by R.V. and F. Fabbrini was provided by Fonds voor Wetenschappelijk Onderzoek Vlaanderen and internal KU Leuven funds (C14/17/109). Primary support for the work by R.H.W. and J.C. was provided by the intramural research program at the NIH. Primary support for the work by A.Y.-S. and P.N.S. was provided by an American Heart Association Western States Affiliate Postdoctoral Fellowship (to A.Y.-S.), Defense Advanced Research Projects Agency (DARPA) Reorganization and Plasticity to Accelerate Injury Recovery (REPAIR; N66001-10-C-2010), and by the UCSF Neuroscience Imaging Center. The work by S.W.E. E.A.H. E.D.R. and M.J. was partially supported by NIH R01 R01NS078127. Primary support for the work of I.E.M. is provided by the National Institute of Mental Health (R01MH110594 and R01MH116937) and the McKnight Foundation. Conception and Design, S. Tremblay, M.J. R.A.G. D.J.O. K.V.S. and M.O.B.; Implementation and Logistics, S. Tremblay and M.J.; Data Contribution, S. Tremblay, A. Angelucci, A.M.C. F. Fabbrini, L.N. C.S. M.A.B. D.M.-H. R.D. L.A. H.X. R.R. K.K. A.R.A. S.R.D. S. Palfi, J.L.S. R. Janz, V.D. N.F. M.K. M.G.F. A. Galvan, Y.-S.S. A. Gail, X.H. D.L.A. M.J.C. H.A. K.M. O.H. E.D.R. S.W.E. E.H. M.J. A. Afraz, A.K. S.S.S. R.A.G. S.G. J.H.R.M. I.E.M. R.S.M. C.I.P. M.M.C. R.M.F. A.W.R. C.K. M.O.-R. M.C.S. W.R.S. W.S. G.B. S.C. Y.C. M.P.W. E.S. M.N.S. C.R.F. D.J.O. K.D. K.V.S. M.O.B. H.G.E.-N. M.A.S. K.-i.I. M.M. M.T. N.J. R. Jiang, S. Tang, M.A.G. A.T. J.H. H.S. S. Treue, P.F.B. W.V. F. Federer. R.V. R.H.W. A.Y.-S. P.N.S. J.D. D.L.S. and J.J.D.; Data Analysis, S. Tremblay; Drafting of the Manuscript, S. Tremblay, A. Angelucci, D.M.-H. R.R. K.K. A. Galvan, R.A.G. J.M.T. M.M.C. R.M.F. A.W.R. M.O.B. M.A.S. N.J. R. Jiang, S. Tang, P.F.B. W.V. F. Federer, R.V. A.Y.-S. P.N.S. J.D. D.L.S. R.C. and M.A.G.E.; Critical Review and Editing of the Manuscript, S. Tremblay, A. Angelucci, C.S. F. Fabbrini, M.A.B. R.C. R.R. K.K. M.G.F. A. Galvan, Y.-S.S. A. Gail, T.W. M.J. A.K. S.S.S. R.A.G. J.M.T. S.G. J.H.R.M. S. Palfi, S.S. R.S.M. C.I.P. M.M.C. R.M.F. A.W.R. Y.C. M.P.W. E.S. M.N.S. D.J.O. K.V.S. M.O.B. H.G.E.-N. M.A.S. K.-i.I. M.M. M.T. J.H. H.S. S. Treue, P.F.B. W.V. F. Federer, R.V. A.Y.-S. P.N.S. J.D. D.L.S. D.M.-H. J.J.D. S.R.D. A.R.A. V.D. N.F. M.K. O.H. A. Aschner, A.K. M.L.P. M.A.G.E. C.R.F. C. Ramakrishnan. K.D. K.V.S. N.J. R. Jiang, S. Tang, R.W. J.C. and M.C.S. S. Palfi received consulting honorarium from OxfordBiomedica. K.V.S. is a consultant for Neuralink and is on the scientific advisory board for CTRL-Labs, MIND-X, Inscopix, and Heal. These entities did not support this work. P.N.S. has financial interests in Neuralink, a company developing clinical therapies using brain stimulation. Funding Information: This manuscript was inspired by the PRIME-DE NeuroResource authored by Milham et al. (2018) . We would like to thank the Jazayeri lab for the initial impetus for this collaboration and the MIT group (DiCarlo, Desimone, and Jazayeri labs) for providing the first in-house database of optogenetics experiments in NHPs that was used as a backbone for the current initiative. We are grateful to the Open Science Framework for hosting the database. Primary support for the work by M.L.P. and S. Tremblay is provided by the Charles E. Kaufman Foundation and the Canada Banting Fellowship . Primary support for A. Angelucci{\textquoteright}s lab is provided by the NIH ( R01 EY026812 , R01 EY019743 , and BRAIN U01 NS099702 ) and the NSF ( IOS 1755431 ). Support for L.N. is additionally provided by an NIH K99 grant ( EY029374 ). Support for the work by A. Afraz (in part) came from the Intramural Research Program of the NIMH ( ZIAMH002958 ). Support for the work contributed by M.A.B. was provided by NIH R01 EY013962 and R21 EY024516 . R.D. acknowledges funding from NIH grant R01EY029666 . Primary support for the work by J.D. is provided by the National Natural Science Foundation of China ( 31600870 ), the Youth Innovation Promotion Association CAS ( 2017120 ), and the Chinese Academy of Sciences International Partnership Program ( 172644KYSB20170004 ). Primary support for the work by D.L.S. and J.D. is provided by Defense Advanced Research Projects Agency (DARPA) Biological Technology Office (BTO) “REPAIR{\textquoteright}{\textquoteright} award N66001-10-C-2010 and NIH-EY014681 . Support for the work by the Dragoi/Janz/Spudich labs is provided by the BRAIN Initiative ( 1U01MH109146 to V.D., R. Janz, and J.L.S.). Primary support for the work by N.F. and M.K. is provided by Brain/MINDS ( JP19dm0207001 ) and KAKENHI ( 17H06034 ). Support for the work by the Treue, Gail, and Scherberger labs was provided by the Leibniz Association ( WGL SAW-2014-DPZ-1 ) and the German Research Foundation ( FOR 1847 ). Support for the work by D.L.A., M.J.C., X.H., A. Galvan, Y.S., and T.W. at Emory University is provided by NIH/NINDS ( P50 NS098685 [Udall Center grant]) and a grant from NIH/ORIP to the Yerkes Center ( P51 OD011132 ). Primary support for the work by H.A., K.M., and O.H. is provided by the National Eye Institute (project 1ZIAEY000415-16 ). Primary support for the work by E.D.R., S.W.E., E.H., and M.J. is provided by the National Institutes of Health ( NINDS-NS078127 ). Primary support for the work by A. Aschner., A.K., and S.S.S. was provided by the NIH ( EY026240 ), Fight for Sight , and the Stavros Niarchos Foundation / Research to Prevent Blindness . Primary support for the work by S.G. and J.H.R.M. is provided by NIH R01EY005911 . Primary support for the work by S. Palfi and S.S. is provided by Fondation de France , Oxford Biomedica (Oxford, UK), and ARSC (France). Primary support for the work by R.S.M. and C.I.P. is provided by a Wellcome Trust Investigator Award, European Research Council Consolidator Award ( MECHIDENT ), and NIH NIDCD R01 (with M. Howard at the University of Iowa). Development of this technique was supported by NIH EY022853 to A.W.R. and Gene Stoner. Primary support for the work by C.K., M.O.-R., and M.C.S. is provided by DFG Emmy Noether grant SCHM 2806/1-1 and European Research Council grant OptoVision 637638 . This work was supported by the Wellcome Trust ( 095495 ), European Research Council ( 293549 ), and NIH Caltech Conte Center ( P50MH094258 ). Primary support for the work by the E.S. lab is provided by NIH-BRAIN U01NS099720 , NEI R01EY016454 , and DARPA-NESD-N66001-17-C-4012 . Primary support for the work by C.R.F. and M.N.S. was provided by the Howard Hughes Medical Institute and the National Eye Institute ( R01 EY11378 ). Primary support for the work by D.J.O., K.D., and K.V.S. is provided by an NSF Graduate Research Fellowship, Dr. Regina Casper Stanford Graduate Fellowship, Defense Advanced Research Projects Agency (DARPA) Biological Technology Office (BTO) “REPAIR{\textquoteright}{\textquoteright} award N66001-10-C-2010 (to K.V.S. and K.D.), DARPA BTO “NeuroFAST{\textquoteright}{\textquoteright} award W911NF-14-2-0013 (to K.D. and K.V.S.), Simons Foundation Collaboration on the Global Brain awards 325380 and 543045 (to K.V.S.), NIH Director{\textquoteright}s Pioneer Award 8DP1HD075623 (to K.V.S.), and the Howard Hughes Medical Institute (to K.D. and K.V.S.). Primary support for the work of K.I., M.M., and M.T. was provided by the Ministry of Education, Science, Sports, Culture, and Technology of Japan , the Japan Science and Technology Agency , and the Japan Agency for Medical Research and Development . Primary support for the work by N.J., R. Jiang, and S. Tang is provided by the National Natural Science Foundation of China and the National Basic Research Program of China . Primary support for the work by M.A.G. and A.T. is provided by the Medical Research Council . Primary support for the work by W.V. and P.F.B. is provided by the Research Foundation Flanders (FWO-Flanders), internal KU Leuven funds ( C14/17/109 ), and the European Union Horizon 2020 Framework Program for Research and Innovation under grant agreement 785907 . Primary support for the work by R.V. and F. Fabbrini was provided by Fonds voor Wetenschappelijk Onderzoek Vlaanderen and internal KU Leuven funds ( C14/17/109 ). Primary support for the work by R.H.W. and J.C. was provided by the intramural research program at the NIH . Primary support for the work by A.Y.-S. and P.N.S. was provided by an American Heart Association Western States Affiliate Postdoctoral Fellowship (to A.Y.-S.), Defense Advanced Research Projects Agency (DARPA) Reorganization and Plasticity to Accelerate Injury Recovery (REPAIR; N66001-10-C-2010 ), and by the UCSF Neuroscience Imaging Center . The work by S.W.E., E.A.H., E.D.R., and M.J. was partially supported by NIH R01 R01NS078127 . Primary support for the work of I.E.M. is provided by the National Institute of Mental Health ( R01MH110594 and R01MH116937 ) and the McKnight Foundation. Publisher Copyright: {\textcopyright} 2020 Elsevier Inc.",

year = "2020",

month = dec,

day = "23",

doi = "10.1016/j.neuron.2020.09.027",

language = "English",

volume = "108",

pages = "1075--1090.e6",

journal = "Neuron",

issn = "0896-6273",

number = "6",

}

Tremblay, S, Acker, L, Afraz, A, Albaugh, DL, Amita, H, Andrei, AR, Angelucci, A, Aschner, A, Balan, PF, Basso, MA, Benvenuti, G, Bohlen, MO, Caiola, MJ, Calcedo, R, Cavanaugh, J, Chen, Y, Chen, S, Chernov, MM, Clark, AM, Dai, J, Debes, SR, Deisseroth, K, Desimone, R, Dragoi, V, Egger, SW, Eldridge, MAG, El-Nahal, HG, Fabbrini, F, Federer, F, Fetsch, CR, Fortuna, MG, Friedman, RM, Fujii, N, Gail, A, Galvan, A, Ghosh, S, Gieselmann, MA, Gulli, RA, Hikosaka, O, Hosseini, EA, Hu, X, Hüer, J, Inoue, KI, Janz, R, Jazayeri, M, Jiang, R, Ju, N, Kar, K, Klein, C, Kohn, A, Komatsu, M, Maeda, K, Martinez-Trujillo, JC, Matsumoto, M, Maunsell, JHR, Mendoza-Halliday, D, Monosov, IE, Muers, RS, Nurminen, L, Ortiz-Rios, M, O'Shea, DJ, Palfi, S, Petkov, CI, Pojoga, S, Rajalingham, R, Ramakrishnan, C, Remington, ED, Revsine, C, Roe, AW, Sabes, PN, Saunders, RC, Scherberger, H, Schmid, MC, Schultz, W, Seidemann, E, Senova, YS, Shadlen, MN, Sheinberg, DL, Siu, C, Smith, Y, Solomon, SS, Sommer, MA, Spudich, JL, Stauffer, WR, Takada, M, Tang, S, Thiele, A, Treue, S, Vanduffel, W, Vogels, R, Whitmire, MP, Wichmann, T, Wurtz, RH, Xu, H, Yazdan-Shahmorad, A, Shenoy, KV, DiCarlo, JJ & Platt, ML 2020, 'An Open Resource for Non-human Primate Optogenetics', Neuron, vol. 108, no. 6, pp. 1075-1090.e6. https://doi.org/10.1016/j.neuron.2020.09.027

TY - JOUR

T1 - An Open Resource for Non-human Primate Optogenetics

AU - Tremblay, Sébastien

AU - Acker, Leah

AU - Afraz, Arash

AU - Albaugh, Daniel L.

AU - Amita, Hidetoshi

AU - Andrei, Ariana R.

AU - Angelucci, Alessandra

AU - Aschner, Amir

AU - Balan, Puiu F.

AU - Basso, Michele A.

AU - Benvenuti, Giacomo

AU - Bohlen, Martin O.

AU - Caiola, Michael J.

AU - Calcedo, Roberto

AU - Cavanaugh, James

AU - Chen, Yuzhi

AU - Chen, Spencer

AU - Chernov, Mykyta M.

AU - Clark, Andrew M.

AU - Dai, Ji

AU - Debes, Samantha R.

AU - Deisseroth, Karl

AU - Desimone, Robert

AU - Dragoi, Valentin

AU - Egger, Seth W.

AU - Eldridge, Mark A.G.

AU - El-Nahal, Hala G.

AU - Fabbrini, Francesco

AU - Federer, Frederick

AU - Fetsch, Christopher R.

AU - Fortuna, Michal G.

AU - Friedman, Robert M.

AU - Fujii, Naotaka

AU - Gail, Alexander

AU - Galvan, Adriana

AU - Ghosh, Supriya

AU - Gieselmann, Marc Alwin

AU - Gulli, Roberto A.

AU - Hikosaka, Okihide

AU - Hosseini, Eghbal A.

AU - Hu, Xing

AU - Hüer, Janina

AU - Inoue, Ken ichi

AU - Janz, Roger

AU - Jazayeri, Mehrdad

AU - Jiang, Rundong

AU - Ju, Niansheng

AU - Kar, Kohitij

AU - Klein, Carsten

AU - Kohn, Adam

AU - Komatsu, Misako

AU - Maeda, Kazutaka

AU - Martinez-Trujillo, Julio C.

AU - Matsumoto, Masayuki

AU - Maunsell, John H.R.

AU - Mendoza-Halliday, Diego

AU - Monosov, Ilya E.

AU - Muers, Ross S.

AU - Nurminen, Lauri

AU - Ortiz-Rios, Michael

AU - O'Shea, Daniel J.

AU - Palfi, Stéphane

AU - Petkov, Christopher I.

AU - Pojoga, Sorin

AU - Rajalingham, Rishi

AU - Ramakrishnan, Charu

AU - Remington, Evan D.

AU - Revsine, Cambria

AU - Roe, Anna W.

AU - Sabes, Philip N.

AU - Saunders, Richard C.

AU - Scherberger, Hansjörg

AU - Schmid, Michael C.

AU - Schultz, Wolfram

AU - Seidemann, Eyal

AU - Senova, Yann Suhan

AU - Shadlen, Michael N.

AU - Sheinberg, David L.

AU - Siu, Caitlin

AU - Smith, Yoland

AU - Solomon, Selina S.

AU - Sommer, Marc A.

AU - Spudich, John L.

AU - Stauffer, William R.

AU - Takada, Masahiko

AU - Tang, Shiming

AU - Thiele, Alexander

AU - Treue, Stefan

AU - Vanduffel, Wim

AU - Vogels, Rufin

AU - Whitmire, Matthew P.

AU - Wichmann, Thomas

AU - Wurtz, Robert H.

AU - Xu, Haoran

AU - Yazdan-Shahmorad, Azadeh

AU - Shenoy, Krishna V.

AU - DiCarlo, James J.

AU - Platt, Michael L.

N1 - Funding Information: This manuscript was inspired by the PRIME-DE NeuroResource authored by Milham et al. (2018). We would like to thank the Jazayeri lab for the initial impetus for this collaboration and the MIT group (DiCarlo, Desimone, and Jazayeri labs) for providing the first in-house database of optogenetics experiments in NHPs that was used as a backbone for the current initiative. We are grateful to the Open Science Framework for hosting the database. Primary support for the work by M.L.P. and S. Tremblay is provided by the Charles E. Kaufman Foundation and the Canada Banting Fellowship. Primary support for A. Angelucci's lab is provided by the NIH (R01 EY026812, R01 EY019743, and BRAIN U01 NS099702) and the NSF (IOS 1755431). Support for L.N. is additionally provided by an NIH K99 grant (EY029374). Support for the work by A. Afraz (in part) came from the Intramural Research Program of the NIMH (ZIAMH002958). Support for the work contributed by M.A.B. was provided by NIH R01 EY013962 and R21 EY024516. R.D. acknowledges funding from NIH grant R01EY029666. Primary support for the work by J.D. is provided by the National Natural Science Foundation of China (31600870), the Youth Innovation Promotion Association CAS (2017120), and the Chinese Academy of Sciences International Partnership Program (172644KYSB20170004). Primary support for the work by D.L.S. and J.D. is provided by Defense Advanced Research Projects Agency (DARPA) Biological Technology Office (BTO) “REPAIR’’ award N66001-10-C-2010 and NIH-EY014681. Support for the work by the Dragoi/Janz/Spudich labs is provided by the BRAIN Initiative (1U01MH109146 to V.D. R. Janz, and J.L.S.). Primary support for the work by N.F. and M.K. is provided by Brain/MINDS (JP19dm0207001) and KAKENHI (17H06034). Support for the work by the Treue, Gail, and Scherberger labs was provided by the Leibniz Association (WGL SAW-2014-DPZ-1) and the German Research Foundation (FOR 1847). Support for the work by D.L.A. M.J.C. X.H. A. Galvan, Y.S. and T.W. at Emory University is provided by NIH/NINDS (P50 NS098685 [Udall Center grant]) and a grant from NIH/ORIP to the Yerkes Center (P51 OD011132). Primary support for the work by H.A. K.M. and O.H. is provided by the National Eye Institute (project 1ZIAEY000415-16). Primary support for the work by E.D.R. S.W.E. E.H. and M.J. is provided by the National Institutes of Health (NINDS-NS078127). Primary support for the work by A. Aschner. A.K. and S.S.S. was provided by the NIH (EY026240), Fight for Sight, and the Stavros Niarchos Foundation/Research to Prevent Blindness. Primary support for the work by S.G. and J.H.R.M. is provided by NIH R01EY005911. Primary support for the work by S. Palfi and S.S. is provided by Fondation de France, Oxford Biomedica (Oxford, UK), and ARSC (France). Primary support for the work by R.S.M. and C.I.P. is provided by a Wellcome Trust Investigator Award, European Research Council Consolidator Award (MECHIDENT), and NIH NIDCD R01 (with M. Howard at the University of Iowa). Development of this technique was supported by NIH EY022853 to A.W.R. and Gene Stoner. Primary support for the work by C.K. M.O.-R. and M.C.S. is provided by DFG Emmy Noether grant SCHM 2806/1-1 and European Research Council grant OptoVision 637638. This work was supported by the Wellcome Trust (095495), European Research Council (293549), and NIH Caltech Conte Center (P50MH094258). Primary support for the work by the E.S. lab is provided by NIH-BRAIN U01NS099720, NEI R01EY016454, and DARPA-NESD-N66001-17-C-4012. Primary support for the work by C.R.F. and M.N.S. was provided by the Howard Hughes Medical Institute and the National Eye Institute (R01 EY11378). Primary support for the work by D.J.O. K.D. and K.V.S. is provided by an NSF Graduate Research Fellowship, Dr. Regina Casper Stanford Graduate Fellowship, Defense Advanced Research Projects Agency (DARPA) Biological Technology Office (BTO) “REPAIR’’ award N66001-10-C-2010 (to K.V.S. and K.D.), DARPA BTO “NeuroFAST’’ award W911NF-14-2-0013 (to K.D. and K.V.S.), Simons Foundation Collaboration on the Global Brain awards 325380 and 543045 (to K.V.S.), NIH Director's Pioneer Award 8DP1HD075623 (to K.V.S.), and the Howard Hughes Medical Institute (to K.D. and K.V.S.). Primary support for the work of K.I. M.M. and M.T. was provided by the Ministry of Education, Science, Sports, Culture, and Technology of Japan, the Japan Science and Technology Agency, and the Japan Agency for Medical Research and Development. Primary support for the work by N.J. R. Jiang, and S. Tang is provided by the National Natural Science Foundation of China and the National Basic Research Program of China. Primary support for the work by M.A.G. and A.T. is provided by the Medical Research Council. Primary support for the work by W.V. and P.F.B. is provided by the Research Foundation Flanders (FWO-Flanders), internal KU Leuven funds (C14/17/109), and the European Union Horizon 2020 Framework Program for Research and Innovation under grant agreement 785907. Primary support for the work by R.V. and F. Fabbrini was provided by Fonds voor Wetenschappelijk Onderzoek Vlaanderen and internal KU Leuven funds (C14/17/109). Primary support for the work by R.H.W. and J.C. was provided by the intramural research program at the NIH. Primary support for the work by A.Y.-S. and P.N.S. was provided by an American Heart Association Western States Affiliate Postdoctoral Fellowship (to A.Y.-S.), Defense Advanced Research Projects Agency (DARPA) Reorganization and Plasticity to Accelerate Injury Recovery (REPAIR; N66001-10-C-2010), and by the UCSF Neuroscience Imaging Center. The work by S.W.E. E.A.H. E.D.R. and M.J. was partially supported by NIH R01 R01NS078127. Primary support for the work of I.E.M. is provided by the National Institute of Mental Health (R01MH110594 and R01MH116937) and the McKnight Foundation. Conception and Design, S. Tremblay, M.J. R.A.G. D.J.O. K.V.S. and M.O.B.; Implementation and Logistics, S. Tremblay and M.J.; Data Contribution, S. Tremblay, A. Angelucci, A.M.C. F. Fabbrini, L.N. C.S. M.A.B. D.M.-H. R.D. L.A. H.X. R.R. K.K. A.R.A. S.R.D. S. Palfi, J.L.S. R. Janz, V.D. N.F. M.K. M.G.F. A. Galvan, Y.-S.S. A. Gail, X.H. D.L.A. M.J.C. H.A. K.M. O.H. E.D.R. S.W.E. E.H. M.J. A. Afraz, A.K. S.S.S. R.A.G. S.G. J.H.R.M. I.E.M. R.S.M. C.I.P. M.M.C. R.M.F. A.W.R. C.K. M.O.-R. M.C.S. W.R.S. W.S. G.B. S.C. Y.C. M.P.W. E.S. M.N.S. C.R.F. D.J.O. K.D. K.V.S. M.O.B. H.G.E.-N. M.A.S. K.-i.I. M.M. M.T. N.J. R. Jiang, S. Tang, M.A.G. A.T. J.H. H.S. S. Treue, P.F.B. W.V. F. Federer. R.V. R.H.W. A.Y.-S. P.N.S. J.D. D.L.S. and J.J.D.; Data Analysis, S. Tremblay; Drafting of the Manuscript, S. Tremblay, A. Angelucci, D.M.-H. R.R. K.K. A. Galvan, R.A.G. J.M.T. M.M.C. R.M.F. A.W.R. M.O.B. M.A.S. N.J. R. Jiang, S. Tang, P.F.B. W.V. F. Federer, R.V. A.Y.-S. P.N.S. J.D. D.L.S. R.C. and M.A.G.E.; Critical Review and Editing of the Manuscript, S. Tremblay, A. Angelucci, C.S. F. Fabbrini, M.A.B. R.C. R.R. K.K. M.G.F. A. Galvan, Y.-S.S. A. Gail, T.W. M.J. A.K. S.S.S. R.A.G. J.M.T. S.G. J.H.R.M. S. Palfi, S.S. R.S.M. C.I.P. M.M.C. R.M.F. A.W.R. Y.C. M.P.W. E.S. M.N.S. D.J.O. K.V.S. M.O.B. H.G.E.-N. M.A.S. K.-i.I. M.M. M.T. J.H. H.S. S. Treue, P.F.B. W.V. F. Federer, R.V. A.Y.-S. P.N.S. J.D. D.L.S. D.M.-H. J.J.D. S.R.D. A.R.A. V.D. N.F. M.K. O.H. A. Aschner, A.K. M.L.P. M.A.G.E. C.R.F. C. Ramakrishnan. K.D. K.V.S. N.J. R. Jiang, S. Tang, R.W. J.C. and M.C.S. S. Palfi received consulting honorarium from OxfordBiomedica. K.V.S. is a consultant for Neuralink and is on the scientific advisory board for CTRL-Labs, MIND-X, Inscopix, and Heal. These entities did not support this work. P.N.S. has financial interests in Neuralink, a company developing clinical therapies using brain stimulation. Funding Information: This manuscript was inspired by the PRIME-DE NeuroResource authored by Milham et al. (2018) . We would like to thank the Jazayeri lab for the initial impetus for this collaboration and the MIT group (DiCarlo, Desimone, and Jazayeri labs) for providing the first in-house database of optogenetics experiments in NHPs that was used as a backbone for the current initiative. We are grateful to the Open Science Framework for hosting the database. Primary support for the work by M.L.P. and S. Tremblay is provided by the Charles E. Kaufman Foundation and the Canada Banting Fellowship . Primary support for A. Angelucci’s lab is provided by the NIH ( R01 EY026812 , R01 EY019743 , and BRAIN U01 NS099702 ) and the NSF ( IOS 1755431 ). Support for L.N. is additionally provided by an NIH K99 grant ( EY029374 ). Support for the work by A. Afraz (in part) came from the Intramural Research Program of the NIMH ( ZIAMH002958 ). Support for the work contributed by M.A.B. was provided by NIH R01 EY013962 and R21 EY024516 . R.D. acknowledges funding from NIH grant R01EY029666 . Primary support for the work by J.D. is provided by the National Natural Science Foundation of China ( 31600870 ), the Youth Innovation Promotion Association CAS ( 2017120 ), and the Chinese Academy of Sciences International Partnership Program ( 172644KYSB20170004 ). Primary support for the work by D.L.S. and J.D. is provided by Defense Advanced Research Projects Agency (DARPA) Biological Technology Office (BTO) “REPAIR’’ award N66001-10-C-2010 and NIH-EY014681 . Support for the work by the Dragoi/Janz/Spudich labs is provided by the BRAIN Initiative ( 1U01MH109146 to V.D., R. Janz, and J.L.S.). Primary support for the work by N.F. and M.K. is provided by Brain/MINDS ( JP19dm0207001 ) and KAKENHI ( 17H06034 ). Support for the work by the Treue, Gail, and Scherberger labs was provided by the Leibniz Association ( WGL SAW-2014-DPZ-1 ) and the German Research Foundation ( FOR 1847 ). Support for the work by D.L.A., M.J.C., X.H., A. Galvan, Y.S., and T.W. at Emory University is provided by NIH/NINDS ( P50 NS098685 [Udall Center grant]) and a grant from NIH/ORIP to the Yerkes Center ( P51 OD011132 ). Primary support for the work by H.A., K.M., and O.H. is provided by the National Eye Institute (project 1ZIAEY000415-16 ). Primary support for the work by E.D.R., S.W.E., E.H., and M.J. is provided by the National Institutes of Health ( NINDS-NS078127 ). Primary support for the work by A. Aschner., A.K., and S.S.S. was provided by the NIH ( EY026240 ), Fight for Sight , and the Stavros Niarchos Foundation / Research to Prevent Blindness . Primary support for the work by S.G. and J.H.R.M. is provided by NIH R01EY005911 . Primary support for the work by S. Palfi and S.S. is provided by Fondation de France , Oxford Biomedica (Oxford, UK), and ARSC (France). Primary support for the work by R.S.M. and C.I.P. is provided by a Wellcome Trust Investigator Award, European Research Council Consolidator Award ( MECHIDENT ), and NIH NIDCD R01 (with M. Howard at the University of Iowa). Development of this technique was supported by NIH EY022853 to A.W.R. and Gene Stoner. Primary support for the work by C.K., M.O.-R., and M.C.S. is provided by DFG Emmy Noether grant SCHM 2806/1-1 and European Research Council grant OptoVision 637638 . This work was supported by the Wellcome Trust ( 095495 ), European Research Council ( 293549 ), and NIH Caltech Conte Center ( P50MH094258 ). Primary support for the work by the E.S. lab is provided by NIH-BRAIN U01NS099720 , NEI R01EY016454 , and DARPA-NESD-N66001-17-C-4012 . Primary support for the work by C.R.F. and M.N.S. was provided by the Howard Hughes Medical Institute and the National Eye Institute ( R01 EY11378 ). Primary support for the work by D.J.O., K.D., and K.V.S. is provided by an NSF Graduate Research Fellowship, Dr. Regina Casper Stanford Graduate Fellowship, Defense Advanced Research Projects Agency (DARPA) Biological Technology Office (BTO) “REPAIR’’ award N66001-10-C-2010 (to K.V.S. and K.D.), DARPA BTO “NeuroFAST’’ award W911NF-14-2-0013 (to K.D. and K.V.S.), Simons Foundation Collaboration on the Global Brain awards 325380 and 543045 (to K.V.S.), NIH Director’s Pioneer Award 8DP1HD075623 (to K.V.S.), and the Howard Hughes Medical Institute (to K.D. and K.V.S.). Primary support for the work of K.I., M.M., and M.T. was provided by the Ministry of Education, Science, Sports, Culture, and Technology of Japan , the Japan Science and Technology Agency , and the Japan Agency for Medical Research and Development . Primary support for the work by N.J., R. Jiang, and S. Tang is provided by the National Natural Science Foundation of China and the National Basic Research Program of China . Primary support for the work by M.A.G. and A.T. is provided by the Medical Research Council . Primary support for the work by W.V. and P.F.B. is provided by the Research Foundation Flanders (FWO-Flanders), internal KU Leuven funds ( C14/17/109 ), and the European Union Horizon 2020 Framework Program for Research and Innovation under grant agreement 785907 . Primary support for the work by R.V. and F. Fabbrini was provided by Fonds voor Wetenschappelijk Onderzoek Vlaanderen and internal KU Leuven funds ( C14/17/109 ). Primary support for the work by R.H.W. and J.C. was provided by the intramural research program at the NIH . Primary support for the work by A.Y.-S. and P.N.S. was provided by an American Heart Association Western States Affiliate Postdoctoral Fellowship (to A.Y.-S.), Defense Advanced Research Projects Agency (DARPA) Reorganization and Plasticity to Accelerate Injury Recovery (REPAIR; N66001-10-C-2010 ), and by the UCSF Neuroscience Imaging Center . The work by S.W.E., E.A.H., E.D.R., and M.J. was partially supported by NIH R01 R01NS078127 . Primary support for the work of I.E.M. is provided by the National Institute of Mental Health ( R01MH110594 and R01MH116937 ) and the McKnight Foundation. Publisher Copyright: © 2020 Elsevier Inc.

PY - 2020/12/23

Y1 - 2020/12/23

N2 - Optogenetics has revolutionized neuroscience in small laboratory animals, but its effect on animal models more closely related to humans, such as non-human primates (NHPs), has been mixed. To make evidence-based decisions in primate optogenetics, the scientific community would benefit from a centralized database listing all attempts, successful and unsuccessful, of using optogenetics in the primate brain. We contacted members of the community to ask for their contributions to an open science initiative. As of this writing, 45 laboratories around the world contributed more than 1,000 injection experiments, including precise details regarding their methods and outcomes. Of those entries, more than half had not been published. The resource is free for everyone to consult and contribute to on the Open Science Framework website. Here we review some of the insights from this initial release of the database and discuss methodological considerations to improve the success of optogenetic experiments in NHPs.

AB - Optogenetics has revolutionized neuroscience in small laboratory animals, but its effect on animal models more closely related to humans, such as non-human primates (NHPs), has been mixed. To make evidence-based decisions in primate optogenetics, the scientific community would benefit from a centralized database listing all attempts, successful and unsuccessful, of using optogenetics in the primate brain. We contacted members of the community to ask for their contributions to an open science initiative. As of this writing, 45 laboratories around the world contributed more than 1,000 injection experiments, including precise details regarding their methods and outcomes. Of those entries, more than half had not been published. The resource is free for everyone to consult and contribute to on the Open Science Framework website. Here we review some of the insights from this initial release of the database and discuss methodological considerations to improve the success of optogenetic experiments in NHPs.

KW - Gene therapy

KW - Monkey

KW - Monkeys

KW - Non-human primates

KW - Nonhuman primates

KW - Open Science

KW - Optical control

KW - Optogenetic

KW - Optogenetics

KW - Viral vectors

UR - http://www.scopus.com/inward/record.url?scp=85088394211&partnerID=8YFLogxK

U2 - 10.1016/j.neuron.2020.09.027

DO - 10.1016/j.neuron.2020.09.027

M3 - Article

C2 - 33080229

AN - SCOPUS:85088394211

SN - 0896-6273

VL - 108

SP - 1075-1090.e6

JO - Neuron

JF - Neuron

IS - 6

ER -

An Open Resource for Non-human Primate Optogenetics

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