Neural manifolds that orchestrate walking and stopping

Abstract

Walking, stopping and maintaining posture are essential motor behaviors, yet the underlying neural processes remain poorly understood. Here, we investigate neural activity behind locomotion and its walk-to-stop transition. Based on a new theory of the lumbar spinal cord1, 2 we propose and predict that spinal population activity contains limit cycle dynamics to drive walking and fixed-point attractors for stopping. To test these predictions we record neural activity in lumbar cord of freely moving rats using Neuropixels probes3. To control stopping, we stimulate a brainstem nucleus, known to induce motor arrest4-7. We find: During locomotion, the population activity of lumbar spinal neurons exhibits rotational dynamics8-10. These dynamics unfold within a low-dimensional locomotor manifold11, 12, a looping set of trajectories that serves as the repeating signature of locomotion, that also behaves as a limit-cycle attractor. Shortly before stopping, the neural state rapidly changes from the locomotor manifold to a postural fixed point attractor. When kicking the state out of the fixed point using perturbations it shifts to a nearby albeit different fixed point. Repeated stoppings form a local quasi-continuum of fixed points representing various poses - i.e. a postural manifold. These observations are in agreement with our theory, which further indicates the mechanistic roles for subpopulations of spinal interneurons for controlling walking and stopping. Besides explaining the data, our theory makes further predictions to be tested in future experiments.