Chronic, wireless recordings of large-scale brain activity in freely moving rhesus monkeys

ABSTRACT Advances in techniques for recording large-scale brain activity contribute to both the elucidation of neurophysiological principles and the development of brain-machine interfaces

(BMIs). Here we describe a neurophysiological paradigm for performing tethered and wireless large-scale recordings based on movable volumetric three-dimensional (3D) multielectrode implants.

This approach allowed us to isolate up to 1,800 neurons (units) per animal and simultaneously record the extracellular activity of close to 500 cortical neurons, distributed across multiple

cortical areas, in freely behaving rhesus monkeys. The method is expandable, in principle, to thousands of simultaneously recorded channels. It also allows increased recording longevity (5

consecutive years) and recording of a broad range of behaviors, such as social interactions, and BMI paradigms in freely moving primates. We propose that wireless large-scale recordings

could have a profound impact on basic primate neurophysiology research while providing a framework for the development and testing of clinically relevant neuroprostheses. Access through your

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BEING VIEWED BY OTHERS A STEALTHY NEURAL RECORDER FOR THE STUDY OF BEHAVIOUR IN PRIMATES Article Open access 08 November 2024 A HIGH-DENSITY 1,024-CHANNEL PROBE FOR BRAIN-WIDE RECORDINGS IN

NON-HUMAN PRIMATES Article 24 June 2024 BRAIN-WIDE NEURAL RECORDINGS IN MICE NAVIGATING PHYSICAL SPACES ENABLED BY ROBOTIC NEURAL RECORDING HEADSTAGES Article 07 October 2024 REFERENCES *

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_Network_ 9, R53–R78 (1998). Article  CAS  Google Scholar  Download references ACKNOWLEDGEMENTS Awards from the US National Institute of Mental Health (NIMH) DP1MH099903 and the US National

Institute of Neurological Disorders and Stroke (NINDS) R01NS073952 to M.A.L.N. supported this research. We thank L. Oliveira and T. Phillips for their gracious support during all

implantation surgeries and experimental logics. Additionally, many thanks go to S. Halkiotis for her continued help in the manuscript revision and submission process. We also thank T.

Vinholo for performing the extensive histology that is shown in this work and H. Powell for analyzing video data from the free roaming experiment. AUTHOR INFORMATION AUTHORS AND AFFILIATIONS

* Department of Neurobiology, Duke University, Durham, North Carolina, USA David A Schwarz, Mikhail A Lebedev, Timothy L Hanson, Gary Lehew, Jim Meloy, Sankaranarayani Rajangam, Zheng Li, 

Arjun Ramakrishnan, Andrew Tate & Miguel A L Nicolelis * Center for Neuroengineering, Duke University, Durham, North Carolina, USA David A Schwarz, Mikhail A Lebedev, Timothy L Hanson, 

Gary Lehew, Jim Meloy, Sankaranarayani Rajangam, Vivek Subramanian, Peter J Ifft, Zheng Li, Arjun Ramakrishnan, Andrew Tate, Katie Z Zhuang & Miguel A L Nicolelis * Monterey Spine,

Monterey, California, USA Dragan F Dimitrov * Department of Biomedical Engineering, Duke University, Durham, North Carolina, USA Vivek Subramanian, Peter J Ifft, Katie Z Zhuang & Miguel

A L Nicolelis * Department of Psychology and Neuroscience, Duke University, Durham, North Carolina, USA Miguel A L Nicolelis * Edmond and Lily Safra International Institute of Neuroscience

of Natal, Natal, Brazil Miguel A L Nicolelis Authors * David A Schwarz View author publications You can also search for this author inPubMed Google Scholar * Mikhail A Lebedev View author

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CONTRIBUTIONS D.A.S., M.A.L. and M.A.L.N. designed experiments and wrote the paper. D.A.S., V.S., M.A.L. and M.A.L.N. analyzed data. D.A.S., M.A.L., S.R., A.R., P.J.I., A.T., T.L.H. and

K.Z.Z. performed the experiments. D.A.S., J.M. and G.L. designed and constructed animal headcaps and manufactured wireless units. G.L. designed and constructed the microwire recording cubes.

D.A.S. and T.L.H. wrote the wireless software. T.L.H. designed and constructed the wireless system. T.L.H. and Z.L. wrote the BMI software and contributed analysis code. D.F.D. designed and

performed the surgical procedures. CORRESPONDING AUTHOR Correspondence to Miguel A L Nicolelis. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare no competing financial interests.

SUPPLEMENTARY INFORMATION SUPPLEMENTARY TEXT AND FIGURES Supplementary Figures 1–13 and Supplementary Tables 1–4 (PDF 2673 kb) WIRELESS BMI 30 second clip of monkey C performing cursor

control with only brain activity, task overlay showing the cursor on the bottom right corner (MP4 3042 kb) BMI WHEELCHAIR CONTROL Video showing macaque controlling robotic cart end effector

with its cortical activity. (MP4 4466 kb) FREELY MOVING WIRELESS RECORDINGS Sample video showing freely moving macaque with an overlay of firing activity divided into left and right

hemisphere. Sample frames from video show behavior with firing activity overlay. Each square represents the firing activity of a single neuron, averaged over 3 30s bins (video framerate).

(MP4 2210 kb) NEURON WAVEFORM CHRONOLOGY Animation of mean waveforms for a single connector (left hemisphere M1) in monkey M. Transparent colored area represented standard deviation of

waveform. Date of recording is shown on top (note some images can correspond to the same date of recording). (MP4 5537 kb) NEURON WAVEFORM CHRONOLOGY Animation of mean waveforms for a single

connector (left hemisphere M1) in monkey N. Transparent colored area represented standard deviation of waveform. Date of recording is shown on top (note some images can correspond to the

same date of recording). (MP4 3679 kb) RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Schwarz, D., Lebedev, M., Hanson, T. _et al._ Chronic, wireless

recordings of large-scale brain activity in freely moving rhesus monkeys. _Nat Methods_ 11, 670–676 (2014). https://doi.org/10.1038/nmeth.2936 Download citation * Received: 16 May 2013 *

Accepted: 12 March 2014 * Published: 28 April 2014 * Issue Date: June 2014 * DOI: https://doi.org/10.1038/nmeth.2936 SHARE THIS ARTICLE Anyone you share the following link with will be able

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