Hierarchical binding of cognition to action in the human basal ganglia-thalamic circuit

Abstract

Flexible behavior requires binding actions to their underlying cognitive variables, yet classical basal ganglia models emphasize a serial architecture where striatal action selection precedes a pallidothalamic motor gate. We tested this framework by recording single-neuron activity across the human pallidothalamic circuit while participants reported perceptual decisions with confidence-weighted reaching movements. Neurons in globus pallidus externus and internus, subthalamic nucleus, and motor thalamus exhibited sharp activity increases at movement onset that persisted through execution and feedback. Choice and confidence were continuously encoded before, during, and after movement. Population decoding revealed a transformation along the circuit, from dynamic upstream representations to stable, low-dimensional representations downstream, particularly in motor thalamus. After feedback, outcome signals emerged selectively in subthalamic nucleus and motor thalamus. In motor thalamus, confidence and outcome converged into a representation consistent with unsigned reward prediction error. These findings redefine the human pallidothalamic circuit as an interface that binds decision, action, and evaluation during behavior.