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

Calcium imaging has rapidly developed into a powerful tool for recording
from large populations of neurons in vivo. Imaging in rhesus macaque motor
cortex can enable the discovery of new principles of motor cortical
function and can inform the design of next generation brain-computer
interfaces (BCIs). Surface two-photon (2P) 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 (2P) imaging of calcium signals from in macaques engaged in a
motor task. By imaging apical dendrites, some of which originated from
deep layer 5 neurons, as well as superficial cell bodies, 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, which was stable across many weeks.
Combining several technical advances, we developed an optical BCI (oBCI)
driven by these dendritic signals and successfully decoded movement
direction online. By fusing 2P functional imaging with CLARITY volumetric
imaging, we verify that an imaged dendrite, which contributed to oBCI
decoding, originated from a putative Betz cell in motor cortical layer 5.
This approach establishes new opportunities for studying motor control and
designing BCIs.