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

Author:

Trautmann Eric M.,O’Shea Daniel J.ORCID,Sun XuluORCID,Marshel James H.,Crow Ailey,Hsueh Brian,Vesuna Sam,Cofer Lucas,Bohner Gergő,Allen Will,Kauvar Isaac,Quirin Sean,MacDougall Matthew,Chen Yuzhi,Whitmire Matthew P.,Ramakrishnan CharuORCID,Sahani ManeeshORCID,Seidemann EyalORCID,Ryu Stephen I.,Deisseroth KarlORCID,Shenoy Krishna V.ORCID

Abstract

AbstractCalcium 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.

Funder

Howard Hughes Medical Institute

U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke

United States Department of Defense | Defense Advanced Research Projects Agency

Simons Foundation

Publisher

Springer Science and Business Media LLC

Subject

General Physics and Astronomy,General Biochemistry, Genetics and Molecular Biology,General Chemistry

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