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 | |
State | Published - Dec 23 2020 |
Keywords
- Gene therapy
- Monkey
- Monkeys
- Non-human primates
- Nonhuman primates
- Open Science
- Optical control
- Optogenetic
- Optogenetics
- Viral vectors
Fingerprint
Dive into the research topics of 'An Open Resource for Non-human Primate Optogenetics'. Together they form a unique fingerprint.Cite this
- APA
- Author
- BIBTEX
- Harvard
- Standard
- RIS
- Vancouver
}
In: Neuron, Vol. 108, No. 6, 23.12.2020, p. 1075-1090.e6.
Research output: Contribution to journal › Article › peer-review
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 -