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Large-scale brain-wide neural recording in nonhuman primates

View ORCID ProfileEric M. Trautmann, View ORCID ProfileJanis K. Hesse, View ORCID ProfileGabriel M. Stine, View ORCID ProfileRuobing Xia, View ORCID ProfileShude Zhu, View ORCID ProfileDaniel J. O’Shea, Bill Karsh, Jennifer Colonell, View ORCID ProfileFrank F. Lanfranchi, View ORCID ProfileSaurabh Vyas, View ORCID ProfileAndrew Zimnik, View ORCID ProfileNatalie A. Steinmann, View ORCID ProfileDaniel A. Wagenaar, Alexandru Andrei, View ORCID ProfileCarolina Mora Lopez, View ORCID ProfileJohn O’Callaghan, View ORCID ProfileJan Putzeys, View ORCID ProfileBogdan C. Raducanu, View ORCID ProfileMarleen Welkenhuysen, View ORCID ProfileMark Churchland, View ORCID ProfileTirin Moore, View ORCID ProfileMichael Shadlen, View ORCID ProfileKrishna Shenoy, View ORCID ProfileDoris Tsao, View ORCID ProfileBarundeb Dutta, View ORCID ProfileTimothy Harris
doi: https://doi.org/10.1101/2023.02.01.526664
Eric M. Trautmann
1Department of Neuroscience, Columbia University Medical Center, New York, NY, USA
2Zuckerman Institute, Columbia University, New York, NY, USA
3Grossman Center for the Statistics of Mind, Columbia University, New York, NY, USA
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  • For correspondence: emt2177@columbia.edu
Janis K. Hesse
4Department of Molecular and Cell Biology, University of California, Berkeley
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Gabriel M. Stine
5McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, MA
6Department of Brain & Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA
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Ruobing Xia
7Department of Neurobiology, Stanford University, Stanford, CA
8Howard Hughes Medical Institute, Stanford University, Stanford, CA
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Shude Zhu
7Department of Neurobiology, Stanford University, Stanford, CA
8Howard Hughes Medical Institute, Stanford University, Stanford, CA
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Daniel J. O’Shea
9Department of Electrical Engineering, Stanford University, Stanford, CA
10Wu Tsai Neuroscience Institute, Stanford University, Stanford, CA
11Bio-X Institute, Stanford University, Stanford, CA
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Bill Karsh
12Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA, USA
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Jennifer Colonell
12Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA, USA
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Frank F. Lanfranchi
13Computation & Neural Systems, California Institute of Technology, Pasadena, CA
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Saurabh Vyas
2Zuckerman Institute, Columbia University, New York, NY, USA
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Andrew Zimnik
1Department of Neuroscience, Columbia University Medical Center, New York, NY, USA
2Zuckerman Institute, Columbia University, New York, NY, USA
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Natalie A. Steinmann
1Department of Neuroscience, Columbia University Medical Center, New York, NY, USA
2Zuckerman Institute, Columbia University, New York, NY, USA
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Daniel A. Wagenaar
4Department of Molecular and Cell Biology, University of California, Berkeley
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Alexandru Andrei
14IMEC, Leuven, Belgium
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Carolina Mora Lopez
14IMEC, Leuven, Belgium
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John O’Callaghan
14IMEC, Leuven, Belgium
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Jan Putzeys
14IMEC, Leuven, Belgium
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Bogdan C. Raducanu
14IMEC, Leuven, Belgium
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Marleen Welkenhuysen
14IMEC, Leuven, Belgium
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Mark Churchland
1Department of Neuroscience, Columbia University Medical Center, New York, NY, USA
2Zuckerman Institute, Columbia University, New York, NY, USA
3Grossman Center for the Statistics of Mind, Columbia University, New York, NY, USA
15Kavli Institute for Brain Sciences, Columbia University, New York, NY
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Tirin Moore
8Howard Hughes Medical Institute, Stanford University, Stanford, CA
17Neuroscience Graduate Program, Stanford University, Stanford, CA
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Michael Shadlen
1Department of Neuroscience, Columbia University Medical Center, New York, NY, USA
2Zuckerman Institute, Columbia University, New York, NY, USA
15Kavli Institute for Brain Sciences, Columbia University, New York, NY
16Howard Hughes Medical Institute, Columbia University, New York, NY
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Krishna Shenoy
8Howard Hughes Medical Institute, Stanford University, Stanford, CA
9Department of Electrical Engineering, Stanford University, Stanford, CA
10Wu Tsai Neuroscience Institute, Stanford University, Stanford, CA
11Bio-X Institute, Stanford University, Stanford, CA
17Neuroscience Graduate Program, Stanford University, Stanford, CA
18Department of Bioengineering, Stanford University, Stanford, CA
19Department of Neurosurgery, School of Medicine, Stanford University, Stanford, CA
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Doris Tsao
4Department of Molecular and Cell Biology, University of California, Berkeley
20Howard Hughes Medical Institute, Berkeley, CA
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Barundeb Dutta
14IMEC, Leuven, Belgium
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Timothy Harris
12Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA, USA
21Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD
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Abstract

High-density, integrated silicon electrodes have begun to transform systems neuroscience, by enabling large-scale neural population recordings with single cell resolution. Existing technologies, however, have provided limited functionality in nonhuman primate species such as macaques, which offer close models of human cognition and behavior. Here, we report the design, fabrication, and performance of Neuropixels 1.0-NHP, a high channel count linear electrode array designed to enable large-scale simultaneous recording in superficial and deep structures within the macaque or other large animal brain. These devices were fabricated in two versions: 4416 electrodes along a 45 mm shank, and 2496 along a 25 mm shank. For both versions, users can programmably select 384 channels, enabling simultaneous multi-area recording with a single probe. We demonstrate recording from over 3000 single neurons within a session, and simultaneous recordings from over 1000 neurons using multiple probes. This technology represents a significant increase in recording access and scalability relative to existing technologies, and enables new classes of experiments involving fine-grained electrophysiological characterization of brain areas, functional connectivity between cells, and simultaneous brain-wide recording at scale.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • We dedicate this manuscript to Krishna Shenoy (1968-2023), whose visionary leadership set this work in motion. His passion and dedication inspired a generation of neuroscientists and engineers, and his presence will continue to resonate within our field and community.

  • - Fixed Author name typo - Minor typo fixes in manuscript - Added dedication to Krishna Shenoy

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted February 04, 2023.
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Large-scale brain-wide neural recording in nonhuman primates
Eric M. Trautmann, Janis K. Hesse, Gabriel M. Stine, Ruobing Xia, Shude Zhu, Daniel J. O’Shea, Bill Karsh, Jennifer Colonell, Frank F. Lanfranchi, Saurabh Vyas, Andrew Zimnik, Natalie A. Steinmann, Daniel A. Wagenaar, Alexandru Andrei, Carolina Mora Lopez, John O’Callaghan, Jan Putzeys, Bogdan C. Raducanu, Marleen Welkenhuysen, Mark Churchland, Tirin Moore, Michael Shadlen, Krishna Shenoy, Doris Tsao, Barundeb Dutta, Timothy Harris
bioRxiv 2023.02.01.526664; doi: https://doi.org/10.1101/2023.02.01.526664
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Large-scale brain-wide neural recording in nonhuman primates
Eric M. Trautmann, Janis K. Hesse, Gabriel M. Stine, Ruobing Xia, Shude Zhu, Daniel J. O’Shea, Bill Karsh, Jennifer Colonell, Frank F. Lanfranchi, Saurabh Vyas, Andrew Zimnik, Natalie A. Steinmann, Daniel A. Wagenaar, Alexandru Andrei, Carolina Mora Lopez, John O’Callaghan, Jan Putzeys, Bogdan C. Raducanu, Marleen Welkenhuysen, Mark Churchland, Tirin Moore, Michael Shadlen, Krishna Shenoy, Doris Tsao, Barundeb Dutta, Timothy Harris
bioRxiv 2023.02.01.526664; doi: https://doi.org/10.1101/2023.02.01.526664

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