The basal ganglia are fundamental to motor control and their dysfunction is linked to motor deficits1–8. Influential investigations on the primate oculomotor system posited that movement generally depends on transient pauses of tonically firing inhibitory basal ganglia output neurons releasing brainstem motor centres9,10. However, prominent increases in basal ganglia output neuron firing observed during other motor tasks cast doubts on the proposed mechanisms of movement regulation through basal ganglia circuitry11–22. Here we show that basal ganglia output neurons in the mouse substantia nigra pars reticulata (SNr) represent complex forelimb movements with highly granular and dynamic changes in spiking activity, tiling task execution at the population level. Single SNr neurons exhibit movement-specific firing pauses as well as increases, each occurring in concert with precise and different forelimb movements. Combining optogenetics and simultaneous recordings from basal ganglia output and postsynaptic brainstem neurons, we reveal the functional role of these dynamic firing-rate changes in releasing and suppressing movement through downstream targets. Together, our results demonstrate the existence and function of highly specific and temporally precise movement representations in basal ganglia output circuitry. We propose a model in which basal ganglia output neurons fire dynamically to provide granular and bidirectional movement-specific signals for release and suppression of motor programs to downstream circuits.
