Large-scale neural recordings with single neuron resolution using Neuropixels probes in human cortex

Angelique C Paulk^{1

2}, Yoav Kfir³, Arjun R Khanna³, Martina L Mustroph⁴, Eric M Trautmann^{5

6

7

8

9

10

11}, Dan J Soper¹², Sergey D Stavisky^{9

10

13

14}, Marleen Welkenhuysen¹⁵, Barundeb Dutta¹⁵, Krishna V Shenoy^{8

9

10

14

16

17}, Leigh R Hochberg^{12

18

19

20}, R Mark Richardson³, Ziv M Williams^#²¹, Sydney S Cash^#^{22

23}

Affiliations

¹ Center for Neurotechnology and Neurorecovery, Department of Neurology, Massachusetts General Hospital, Boston, MA, USA. apaulk@mgh.harvard.edu.
² Department of Neurology, Harvard Medical School, Boston, MA, USA. apaulk@mgh.harvard.edu.
³ Department of Neurosurgery, Harvard Medical School and Massachusetts General Hospital, Boston, MA, USA.
⁴ Department of Neurosurgery, Harvard Medical School and Brigham & Women's Hospital, Boston, MA, USA.
⁵ Department of Neuroscience, Columbia University Medical Center, New York City, NY, USA.
⁶ Zuckerman Institute, Columbia University, New York City, NY, USA.
⁷ Grossman Center for the Statistics of Mind, Columbia University Medical Center, New York City, NY, USA.
⁸ Department of Electrical Engineering, Stanford University, Stanford, CA, USA.
⁹ Wu Tsai Neurosciences Institute and Bio-X Institute, Stanford University, Stanford, CA, USA.
¹⁰ Howard Hughes Medical Institute at Stanford University, Stanford, CA, USA.
¹¹ Columbia University, New York City, NY, USA.
¹² Center for Neurotechnology and Neurorecovery, Department of Neurology, Massachusetts General Hospital, Boston, MA, USA.
¹³ Department of Neurological Surgery, University of California at Davis, Davis, CA, USA.
¹⁴ Department of Neurosurgery, Stanford University, Stanford, CA, USA.
¹⁵ IMEC, Leuven, Belgium.
¹⁶ Department of Bioengineering, Stanford University, Stanford, CA, USA.
¹⁷ Department of Neurobiology, Stanford University, Stanford, CA, USA.
¹⁸ Department of Neurology, Harvard Medical School, Boston, MA, USA.
¹⁹ VA RR&D Center for Neurorestoration and Neurotechnology, Rehabilitation R&D Service, Providence VA Medical Center, Providence, RI, USA.
²⁰ School of Engineering and Carney Institute for Brain Science, Brown University, Providence, RI, USA.
²¹ Department of Neurosurgery, Harvard Medical School and Massachusetts General Hospital, Boston, MA, USA. zwilliams@mgh.harvard.edu.
²² Center for Neurotechnology and Neurorecovery, Department of Neurology, Massachusetts General Hospital, Boston, MA, USA. scash@mgh.harvard.edu.
²³ Department of Neurology, Harvard Medical School, Boston, MA, USA. scash@mgh.harvard.edu.

^# Contributed equally.

PMID: 35102333
DOI: 10.1038/s41593-021-00997-0

Large-scale neural recordings with single neuron resolution using Neuropixels probes in human cortex

Angelique C Paulk et al. Nat Neurosci. 2022 Feb.

. 2022 Feb;25(2):252-263.

doi: 10.1038/s41593-021-00997-0. Epub 2022 Jan 31.

Authors

Affiliations

¹ Center for Neurotechnology and Neurorecovery, Department of Neurology, Massachusetts General Hospital, Boston, MA, USA. apaulk@mgh.harvard.edu.
² Department of Neurology, Harvard Medical School, Boston, MA, USA. apaulk@mgh.harvard.edu.
³ Department of Neurosurgery, Harvard Medical School and Massachusetts General Hospital, Boston, MA, USA.
⁴ Department of Neurosurgery, Harvard Medical School and Brigham & Women's Hospital, Boston, MA, USA.
⁵ Department of Neuroscience, Columbia University Medical Center, New York City, NY, USA.
⁶ Zuckerman Institute, Columbia University, New York City, NY, USA.
⁷ Grossman Center for the Statistics of Mind, Columbia University Medical Center, New York City, NY, USA.
⁸ Department of Electrical Engineering, Stanford University, Stanford, CA, USA.
⁹ Wu Tsai Neurosciences Institute and Bio-X Institute, Stanford University, Stanford, CA, USA.
¹⁰ Howard Hughes Medical Institute at Stanford University, Stanford, CA, USA.
¹¹ Columbia University, New York City, NY, USA.
¹² Center for Neurotechnology and Neurorecovery, Department of Neurology, Massachusetts General Hospital, Boston, MA, USA.
¹³ Department of Neurological Surgery, University of California at Davis, Davis, CA, USA.
¹⁴ Department of Neurosurgery, Stanford University, Stanford, CA, USA.
¹⁵ IMEC, Leuven, Belgium.
¹⁶ Department of Bioengineering, Stanford University, Stanford, CA, USA.
¹⁷ Department of Neurobiology, Stanford University, Stanford, CA, USA.
¹⁸ Department of Neurology, Harvard Medical School, Boston, MA, USA.
¹⁹ VA RR&D Center for Neurorestoration and Neurotechnology, Rehabilitation R&D Service, Providence VA Medical Center, Providence, RI, USA.
²⁰ School of Engineering and Carney Institute for Brain Science, Brown University, Providence, RI, USA.
²¹ Department of Neurosurgery, Harvard Medical School and Massachusetts General Hospital, Boston, MA, USA. zwilliams@mgh.harvard.edu.
²² Center for Neurotechnology and Neurorecovery, Department of Neurology, Massachusetts General Hospital, Boston, MA, USA. scash@mgh.harvard.edu.
²³ Department of Neurology, Harvard Medical School, Boston, MA, USA. scash@mgh.harvard.edu.

^# Contributed equally.

PMID: 35102333
DOI: 10.1038/s41593-021-00997-0

Abstract

Recent advances in multi-electrode array technology have made it possible to monitor large neuronal ensembles at cellular resolution in animal models. In humans, however, current approaches restrict recordings to a few neurons per penetrating electrode or combine the signals of thousands of neurons in local field potential (LFP) recordings. Here we describe a new probe variant and set of techniques that enable simultaneous recording from over 200 well-isolated cortical single units in human participants during intraoperative neurosurgical procedures using silicon Neuropixels probes. We characterized a diversity of extracellular waveforms with eight separable single-unit classes, with differing firing rates, locations along the length of the electrode array, waveform spatial spread and modulation by LFP events such as inter-ictal discharges and burst suppression. Although some challenges remain in creating a turnkey recording system, high-density silicon arrays provide a path for studying human-specific cognitive processes and their dysfunction at unprecedented spatiotemporal resolution.

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References

1. Jun, J. J. et al. Fully integrated silicon probes for high-density recording of neural activity. Nature 551, 232–236 (2017). - PubMed - PMC - DOI
1. Jia, X. et al. High-density extracellular probes reveal dendritic backpropagation and facilitate neuron classification. J. Neurophysiol. 121, 1831–1847 (2019). - PubMed - DOI
1. Trautmann, E. M. et al. Accurate estimation of neural population dynamics without spike sorting. Neuron 103, 292–308.e4 (2019). - PubMed - PMC - DOI
1. Steinmetz, N. A. et al. Neuropixels 2.0: a miniaturized high-density probe for stable, long-term brain recordings. Science 372, eabf4588 (2021). - PubMed - PMC - DOI
1. Ward, A. A. & Thomas, L. B. The electrical activity of single units in the cerebral cortex of man. Electroencephalogr. Clin. Neurophysiol. 7, 135–136 (1955). - PubMed - DOI

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Large-scale neural recordings with single neuron resolution using Neuropixels probes in human cortex

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Large-scale neural recordings with single neuron resolution using Neuropixels probes in human cortex

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