Basal Ganglia Output Dynamically Controls Skilled Forelimb Kinematics in Real Time

Abstract

The substantia nigra pars reticulata (SNr), the principal output nucleus of the basal ganglia, is traditionally viewed as a binary gate that permits actions through disinhibition. However, this framework fails to explain the fluid, high-dimensional control required for skilled behavior. Using high-resolution 3D kinematic tracking and automated behavioral classification, we show that SNr population activity paradoxically increases during skilled forelimb reaching and scales with motif-specific kinematics. Systematic optogenetic and chemogenetic perturbations reveal that the SNr bidirectionally controls movement vigor and online kinematics. Remarkably, a transient 12.5 ms pause is sufficient to abort a motor program, while a 12.5 ms burst enhances velocity and reshapes trajectories without altering sequence identity. Calcium imaging at single-neuron resolution further confirms that endogenous SNr dynamics represent real-time 3D kinematics. These findings demonstrate that SNr output does not merely gate movement initiation but continuously regulates the stability and kinematic evolution of skilled actions, expanding the functional framework of basal ganglia output from binary selection to the real-time dynamical control of motor execution.