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

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, Yuzhi Chen, Matthew P. Whitmire, Charu Ramakrishnan, Maneesh Sahani, Eyal Seidemann, Stephen I. Ryu, Karl Deisseroth () and Krishna V. Shenoy ()
Additional contact information
Eric M. Trautmann: Stanford University
Daniel J. O’Shea: 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
Matthew P. Whitmire: University of Texas
Charu Ramakrishnan: Stanford University
Maneesh Sahani: University College London
Eyal Seidemann: University of Texas
Stephen I. Ryu: Stanford University
Karl Deisseroth: Stanford University
Krishna V. Shenoy: Stanford University

Nature Communications, 2021, vol. 12, issue 1, 1-20

Abstract: 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.

Date: 2021
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DOI: 10.1038/s41467-021-23884-5

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