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

Nature Methods volume 11, pages 670–676 (2014)Cite this article

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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.

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Figure 1: Recording cubes and primate headcap.
Figure 2: Large-scale activity recordings.
Figure 3: Recording longevity.
Figure 4: Wireless brain-machine interface (monkey C data).
Figure 5: Recordings of freely behaving monkeys.

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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.

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Authors and Affiliations

  1. 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

  2. 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

  3. Monterey Spine, Monterey, California, USA

    Dragan F Dimitrov

  4. Department of Biomedical Engineering, Duke University, Durham, North Carolina, USA

    Vivek Subramanian, Peter J Ifft, Katie Z Zhuang & Miguel A L Nicolelis

  5. Department of Psychology and Neuroscience, Duke University, Durham, North Carolina, USA

    Miguel A L Nicolelis

  6. Edmond and Lily Safra International Institute of Neuroscience of Natal, Natal, Brazil

    Miguel A L Nicolelis

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  1. David A Schwarz
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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.

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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)

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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

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