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Dendritic calcium signals in rhesus macaque motor cortex drive an optical brain-computer interface

Author

Listed:
  • Eric M. Trautmann

    (Stanford University
    Stanford University)

  • Daniel J. O’Shea

    (Stanford University
    Stanford University)

  • Xulu Sun

    (Stanford University)

  • James H. Marshel

    (Stanford University)

  • Ailey Crow

    (Stanford University)

  • Brian Hsueh

    (Stanford University)

  • Sam Vesuna

    (Stanford University)

  • Lucas Cofer

    (Stanford University)

  • Gergő Bohner

    (University College London)

  • Will Allen

    (Stanford University)

  • Isaac Kauvar

    (Stanford University)

  • Sean Quirin

    (Stanford University)

  • Matthew MacDougall

    (Stanford University)

  • Yuzhi Chen

    (University of Texas
    University of Texas
    University of Texas)

  • Matthew P. Whitmire

    (University of Texas
    University of Texas
    University of Texas)

  • Charu Ramakrishnan

    (Stanford University)

  • Maneesh Sahani

    (University College London)

  • Eyal Seidemann

    (University of Texas
    University of Texas
    University of Texas)

  • Stephen I. Ryu

    (Stanford University
    Palo Alto Medical Foundation)

  • Karl Deisseroth

    (Stanford University
    Stanford University
    Stanford University
    Stanford University)

  • Krishna V. Shenoy

    (Stanford University
    Stanford University
    Stanford University
    Stanford University)

Abstract

Calcium imaging is a powerful tool for recording from large populations of neurons in vivo. Imaging in rhesus macaque motor cortex can enable the discovery of fundamental principles of motor cortical function and can inform the design of next generation brain-computer interfaces (BCIs). Surface two-photon imaging, however, cannot presently access somatic calcium signals of neurons from all layers of macaque motor cortex due to photon scattering. Here, we demonstrate an implant and imaging system capable of chronic, motion-stabilized two-photon imaging of neuronal calcium signals from macaques engaged in a motor task. By imaging apical dendrites, we achieved optical access to large populations of deep and superficial cortical neurons across dorsal premotor (PMd) and gyral primary motor (M1) cortices. Dendritic signals from individual neurons displayed tuning for different directions of arm movement. Combining several technical advances, we developed an optical BCI (oBCI) driven by these dendritic signalswhich successfully decoded movement direction online. By fusing two-photon functional imaging with CLARITY volumetric imaging, we verified that many imaged dendrites which contributed to oBCI decoding originated from layer 5 output neurons, including a putative Betz cell. This approach establishes new opportunities for studying motor control and designing BCIs via two photon imaging.

Suggested Citation

  • Eric M. Trautmann & Daniel J. O’Shea & Xulu Sun & James H. Marshel & Ailey Crow & Brian Hsueh & Sam Vesuna & Lucas Cofer & Gergő Bohner & Will Allen & Isaac Kauvar & Sean Quirin & Matthew MacDougall &, 2021. "Dendritic calcium signals in rhesus macaque motor cortex drive an optical brain-computer interface," Nature Communications, Nature, vol. 12(1), pages 1-20, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-23884-5
    DOI: 10.1038/s41467-021-23884-5
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    Cited by:

    1. Jimin Wu & Yuzhi Chen & Ashok Veeraraghavan & Eyal Seidemann & Jacob T. Robinson, 2024. "Mesoscopic calcium imaging in a head-unrestrained male non-human primate using a lensless microscope," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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