Hand Knob Area of Premotor Cortex Represents the Whole Body in a Compositional Way

Francis R Willett; Darrel R Deo; Donald T Avansino; Paymon Rezaii; Leigh R Hochberg; Jaimie M Henderson; Krishna V Shenoy

doi:10.1016/j.cell.2020.02.043

Hand Knob Area of Premotor Cortex Represents the Whole Body in a Compositional Way

Cell. 2020 Apr 16;181(2):396-409.e26. doi: 10.1016/j.cell.2020.02.043. Epub 2020 Mar 26.

Authors

Francis R Willett¹, Darrel R Deo², Donald T Avansino³, Paymon Rezaii³, Leigh R Hochberg⁴, Jaimie M Henderson⁵, Krishna V Shenoy⁶

Affiliations

¹ Department of Neurosurgery, Stanford University, Stanford, CA, USA; Department of Electrical Engineering, Stanford University, Stanford, CA, USA; Howard Hughes Medical Institute at Stanford University, Stanford, CA, USA. Electronic address: fwillett@stanford.edu.
² Department of Neurosurgery, Stanford University, Stanford, CA, USA; Department of Electrical Engineering, Stanford University, Stanford, CA, USA; Department of Mechanical Engineering, Stanford University, Stanford, CA, USA.
³ Department of Neurosurgery, Stanford University, Stanford, CA, USA.
⁴ VA RR&D Center for Neurorestoration and Neurotechnology, Rehabilitation R&D Service, Providence VA Medical Center, Providence, RI, USA; School of Engineering and Carney Institute for Brain Science, Brown University, Providence, RI, USA; Department of Neurology, Harvard Medical School, Boston, MA, USA; Center for Neurotechnology and Neurorecovery, Department of Neurology, Massachusetts General Hospital, Boston, MA, USA.
⁵ Department of Neurosurgery, Stanford University, Stanford, CA, USA; Wu Tsai Neurosciences Institute, Bio-X Program, Stanford University, Stanford, CA, USA.
⁶ Department of Electrical Engineering, Stanford University, Stanford, CA, USA; Department of Bioengineering, Stanford University, Stanford, CA, USA; Department of Neurobiology, Stanford University, Stanford, CA, USA; Howard Hughes Medical Institute at Stanford University, Stanford, CA, USA; Wu Tsai Neurosciences Institute, Bio-X Program, Stanford University, Stanford, CA, USA.

Abstract

Decades after the motor homunculus was first proposed, it is still unknown how different body parts are intermixed and interrelated in human motor cortical areas at single-neuron resolution. Using multi-unit recordings, we studied how face, head, arm, and leg movements are represented in the hand knob area of premotor cortex (precentral gyrus) in people with tetraplegia. Contrary to traditional expectations, we found strong representation of all movements and a partially "compositional" neural code that linked together all four limbs. The code consisted of (1) a limb-coding component representing the limb to be moved and (2) a movement-coding component where analogous movements from each limb (e.g., hand grasp and toe curl) were represented similarly. Compositional coding might facilitate skill transfer across limbs, and it provides a useful framework for thinking about how the motor system constructs movement. Finally, we leveraged these results to create a whole-body intracortical brain-computer interface that spreads targets across all limbs.

Keywords: brain-computer interface; hand knob; microelectrode array; motor cortex; neural coding; skill transfer.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Adult
Brain Mapping
Frontal Lobe / anatomy & histology
Frontal Lobe / physiology*
Human Body
Humans
Motor Cortex / anatomy & histology*
Motor Cortex / metabolism
Motor Cortex / physiology*
Movement / physiology

Abstract

Publication types

MeSH terms

Grants and funding