Localized Tuning Fields for 3D Hand Position in the Primary Motor Cortex and Premotor Cortex of Macaques

Abstract

A central question in motor neuroscience is how the brain represents the state of the limbs to guide volitional movements. While the primate motor cortex is known to encode movement kinematics, such as velocity and direction, whether it also maintains a direct and explicit representation of hand position in 3D space remains debated. To address this, we recorded the activity of single neurons in the primary motor cortex (M1) and dorsal premotor cortex (PMd) of two male rhesus macaques performing a naturalistic, self-paced 3D reach-and-grasp task. We found significant populations of neurons in both M1 (36.2%) and PMd (21.3%) that are robustly tuned to the instantaneous 3D position of the hand. In these neurons, the tuning for hand position—characterized by localized, elongated fields—coexists with tunings for other kinematic variables, reflecting the principle of mixed selectivity. Critically, the spatial organization of these representations differs between the two areas: M1 fields are systematically oriented along cardinal axes and exhibit multiscale spatial clustering, whereas PMd fields are more randomly organized. Furthermore, a small subset of these hand position-tuned cells is sufficient to decode the hand’s 3D trajectory with high fidelity. Our findings demonstrate that an explicit and functionally organized representation of 3D hand position is a fundamental component of primate motor cortex, complementing dynamic motor signals to support high-fidelity motor control.