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

Neuron. 2020 Dec 23;108(6):1075-1090.e6. doi: 10.1016/j.neuron.2020.09.027. Epub 2020 Oct 19.

Authors

Sébastien Tremblay¹, Leah Acker², Arash Afraz³, Daniel L Albaugh⁴, Hidetoshi Amita⁵, Ariana R Andrei⁶, Alessandra Angelucci⁷, Amir Aschner⁸, Puiu F Balan⁹, Michele A Basso¹⁰, Giacomo Benvenuti¹¹, Martin O Bohlen¹², Michael J Caiola⁴, Roberto Calcedo¹³, James Cavanaugh¹⁴, Yuzhi Chen¹¹, Spencer Chen¹¹, Mykyta M Chernov¹⁵, Andrew M Clark⁷, Ji Dai¹⁶, Samantha R Debes⁶, Karl Deisseroth¹⁷, Robert Desimone², Valentin Dragoi⁶, Seth W Egger², Mark A G Eldridge¹⁸, Hala G El-Nahal¹², Francesco Fabbrini¹⁹, Frederick Federer⁷, Christopher R Fetsch²⁰, Michal G Fortuna²¹, Robert M Friedman¹⁵, Naotaka Fujii²², Alexander Gail²³, Adriana Galvan⁴, Supriya Ghosh²⁴, Marc Alwin Gieselmann²⁵, Roberto A Gulli²⁶, Okihide Hikosaka⁵, Eghbal A Hosseini², Xing Hu⁴, Janina Hüer²¹, Ken-Ichi Inoue²⁷, Roger Janz⁶, Mehrdad Jazayeri², Rundong Jiang²⁸, Niansheng Ju²⁸, Kohitij Kar², Carsten Klein²⁹, Adam Kohn³⁰, Misako Komatsu²², Kazutaka Maeda⁵, Julio C Martinez-Trujillo³¹, Masayuki Matsumoto³², John H R Maunsell²⁴, Diego Mendoza-Halliday², Ilya E Monosov³³, Ross S Muers²⁵, Lauri Nurminen⁷, Michael Ortiz-Rios³⁴, Daniel J O'Shea³⁵, Stéphane Palfi³⁶, Christopher I Petkov²⁵, Sorin Pojoga⁶, Rishi Rajalingham², Charu Ramakrishnan³⁷, Evan D Remington², Cambria Revsine³⁸, Anna W Roe³⁹, Philip N Sabes⁴⁰, Richard C Saunders¹⁸, Hansjörg Scherberger²³, Michael C Schmid⁴¹, Wolfram Schultz⁴², Eyal Seidemann¹¹, Yann-Suhan Senova³⁶, Michael N Shadlen⁴³, David L Sheinberg⁴⁴, Caitlin Siu⁷, Yoland Smith⁴, Selina S Solomon⁸, Marc A Sommer¹², John L Spudich⁴⁵, William R Stauffer⁴⁶, Masahiko Takada⁴⁷, Shiming Tang²⁸, Alexander Thiele²⁵, Stefan Treue²³, Wim Vanduffel⁴⁸, Rufin Vogels¹⁹, Matthew P Whitmire¹¹, Thomas Wichmann⁴, Robert H Wurtz¹⁴, Haoran Xu², Azadeh Yazdan-Shahmorad⁴⁹, Krishna V Shenoy⁵⁰, James J DiCarlo², Michael L Platt⁵¹

Affiliations

¹ Department of Neuroscience, University of Pennsylvania, Philadelphia, PA 19104, USA. Electronic address: strem@pennmedicine.upenn.edu.
² McGovern Institute for Brain Research, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
³ National Institute of Mental Health, National Institutes of Health, Bethesda, MD 20892, USA.
⁴ Yerkes National Primate Research Center, Morris K. Udall Center of Excellence for Parkinson's Disease, Department of Neurology, Emory University, GA 30329, USA.
⁵ Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, MD 20892, USA.
⁶ Department of Neurobiology and Anatomy, McGovern Medical School, University of Texas-Houston, Houston, TX 77030, USA.
⁷ Department of Ophthalmology, Moran Eye Institute, University of Utah, Salt Lake City, UT 84132, USA.
⁸ Dominik P. Purpura Department of Neuroscience, Albert Einstein College of Medicine, Bronx, NY 10461, USA.
⁹ Laboratory of Neuro- and Psychophysiology, KU Leuven, 3000 Leuven, Belgium.
¹⁰ Departments of Psychiatry and Biobehavioral Sciences and Neurobiology, UCLA, Los Angeles, CA 90095, USA.
¹¹ Departments of Psychology and Neuroscience, Center for Perceptual Systems, University of Texas, Austin, TX 78712, USA.
¹² Department of Biomedical Engineering, Duke University, Durham, NC 27708, USA.
¹³ Gene Therapy Program, Department of Medicine, University of Pennsylvania, Philadelphia, PA 19014, USA.
¹⁴ Laboratory of Sensorimotor Research, National Eye Institute, NIH, Bethesda, MD 20982, USA.
¹⁵ Division of Neuroscience, Oregon National Primate Resource Center, Oregon Health and Science University, Beaverton, OR 97006, USA.
¹⁶ CAS Key Laboratory of Brain Connectome and Manipulation, The Brain Cognition and Brain Disease Institute, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen-Hong Kong Institute of Brain Science, Shenzhen 518055, China.
¹⁷ Neuroscience Program, Departments of Bioengineering, Psychiatry, and Behavioral Science, Wu Tsai Neurosciences Institute, Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305, USA.
¹⁸ Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD 20892, USA.
¹⁹ Laboratory of Neuro- and Psychophysiology, KU Leuven, 3000 Leuven, Belgium; Leuven Brain Institute, KU Leuven, 3000 Leuven, Belgium.
²⁰ The Solomon H. Snyder Department of Neuroscience & Zanvyl Krieger Mind/Brain Institute, Johns Hopkins University, Baltimore, MD 21218, USA.
²¹ German Primate Center - Leibniz Institute for Primate Research, 37077 Göttingen, Germany.
²² Laboratory for Adaptive Intelligence, RIKEN Brain Science Institute, Wako, Saitama 351-0198, Japan.
²³ German Primate Center - Leibniz Institute for Primate Research, 37077 Göttingen, Germany; Bernstein Center for Computational Neuroscience, Göttingen, Germany; Faculty for Biology and Psychology, University of Göttingen, Göttingen, Germany; Leibniz Science Campus Primate Cognition, Göttingen, Germany.
²⁴ Department of Neurobiology and Grossman Institute for Neuroscience, Quantitative Biology and Human Behavior, University of Chicago, Chicago, IL 60637, USA.
²⁵ Biosciences Institute, Faculty of Medical Sciences, Newcastle University, Newcastle NE2 4HH, UK.
²⁶ Zuckerman Institute, Columbia University, New York, NY 10027, USA; Center for Theoretical Neuroscience, Columbia University, New York, NY 10027, USA.
²⁷ Systems Neuroscience Section, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan; PRESTO, Japan Science and Technology Agency, Kawaguchi, Saitama 332-0012, Japan.
²⁸ School of Life Sciences, Peking University, Beijing 100871, China.
²⁹ Max Planck Institute for Biological Cybernetics, Tübingen, Germany.
³⁰ Dominik P. Purpura Department of Neuroscience, Albert Einstein College of Medicine, Bronx, NY 10461, USA; Department of Ophthalmology and Visual Sciences, Albert Einstein College of Medicine, Bronx, NY 10461, USA; Department of Systems and Computational Biology, Albert Einstein College of Medicine, Bronx, NY 10461, USA.
³¹ Robarts Research Institute, Schulich School of Medicine and Dentistry, University of Western Ontario, London, ON, Canada; Brain and Mind Institute, University of Western Ontario, London, ON, Canada.
³² Division of Biomedical Science, Faculty of Medicine, University of Tsukuba, Tsukuba, Ibaraki 305-8575, Japan; Transborder Medical Research Center, University of Tsukuba, Tsukuba, Ibaraki 305-8577, Japan.
³³ Department of Neuroscience, Biomedical Engineering, Electrical Engineering, Neurosurgery and Pain Center, Washington University, St. Louis, MO 63110, USA.
³⁴ German Primate Center - Leibniz Institute for Primate Research, 37077 Göttingen, Germany; Leibniz Science Campus Primate Cognition, Göttingen, Germany; Biosciences Institute, Faculty of Medical Sciences, Newcastle University, Newcastle NE2 4HH, UK.
³⁵ Department of Electrical Engineering, Wu Tsai Neurosciences Institute, and Bio-X Institute, and Neuroscience Graduate Program, Stanford University, Stanford, CA 94305, USA.
³⁶ Department of Neurosurgery, Assistance Publique-Hopitaux de Paris (APHP), U955 INSERM IMRB eq.15, University of Paris 12 UPEC, Faculté de Médecine, Créteil 94010, France.
³⁷ Department of Bioengineering, Stanford University, Stanford, CA 94305, USA.
³⁸ Department of Neuroscience, University of Pennsylvania, Philadelphia, PA 19104, USA; Laboratory of Brain and Cognition, National Institute of Mental Health, National Institutes of Health, Bethesda, MD 20814, USA.
³⁹ Division of Neuroscience, Oregon National Primate Resource Center, Oregon Health and Science University, Beaverton, OR 97006, USA; Interdisciplinary Institute of Neuroscience and Technology, Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou 310029, China; Key Laboratory of Biomedical Engineering of the Ministry of Education, Zhejiang University, Hangzhou 310029, China.
⁴⁰ Center for Integrative Neuroscience, University of California, San Francisco, San Francisco, CA 94158, USA.
⁴¹ Biosciences Institute, Faculty of Medical Sciences, Newcastle University, Newcastle NE2 4HH, UK; Department of Neurosciences and Movement Sciences, Faculty of Science and Medicine, University of Fribourg, 1700 Fribourg, Switzerland.
⁴² Department of Physiology, Development of Neuroscience, University of Cambridge, Cambridge CB3 0LT, UK.
⁴³ Department of Neuroscience, Mortimer B. Zuckerman Mind Brain Behavior Institute, The Kavli Institute for Brain Science & Howard Hughes Medical Institute, Columbia University, NY 10027, USA.
⁴⁴ Department of Neuroscience and Carney Institute for Brain Science, Brown University, Providence, RI 02912, USA.
⁴⁵ Department of Biochemistry and Molecular Biology, McGovern Medical School, The University of Texas-Houston, Houston, TX 77030, USA.
⁴⁶ Systems Neuroscience Institute, Department of Neurobiology, University of Pittsburgh, Pittsburgh, PA 15260, USA.
⁴⁷ Systems Neuroscience Section, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan.
⁴⁸ Laboratory of Neuro- and Psychophysiology, KU Leuven, 3000 Leuven, Belgium; Leuven Brain Institute, KU Leuven, 3000 Leuven, Belgium; MGH Martinos Center, Charlestown, MA 02129, USA; Harvard Medical School, Boston, MA 02144, USA.
⁴⁹ Center for Integrative Neuroscience, University of California, San Francisco, San Francisco, CA 94158, USA; Departments of Bioengineering and Electrical and Computer Engineering, Washington National Primate Research Center, University of Washington, Seattle, WA 98105, USA.
⁵⁰ Departments of Electrical Engineering, Bioengineering, and Neurobiology, Wu Tsai Neurosciences Institute and Bio-X Institute, Neuroscience Graduate Program, and Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305, USA.
⁵¹ Department of Neuroscience, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Psychology, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Marketing, Wharton School, University of Pennsylvania, Philadelphia, PA 19104, USA.

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.

Publication types

Research Support, N.I.H., Extramural
Research Support, N.I.H., Intramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animals
Brain*
Neurons*
Neurosciences
Optogenetics / methods*
Primates*

Abstract

Publication types

MeSH terms

Grants and funding