Motor Cortex in Theory and Practice

A central question in motor physiology has been whether motor cortex activity resembles muscle activity, and if not, why not? Over fifty years, extensive observations have failed to provide a concise answer, and the topic remains much debated. To provide a different perspective, we employed a novel behavioral paradigm that affords extensive comparison between time-evolving neural and muscle activity. Single motor-cortex neurons displayed many muscle-like properties, but the structure of population activity was not muscle-like. Unlike muscle activity, neural activity was structured to avoid ’trajectory tangling’: moments where similar activity patterns led to dissimilar future patterns. Avoidance of trajectory tangling was present across tasks and species. Network models revealed a potential reason for this consistent feature: low tangling confers noise robustness. Remarkably, we were able to predict motor cortex activity from muscle activity alone, by leveraging the hypothesis that muscle-like commands are embedded in additional structure that yields low tangling. Our results argue that motor cortex embeds descending commands in additional structure that ensure low tangling, and thus noise-robustness. The dominant structure in motor cortex may thus serve not a representational function (encoding specific variables) but a computational function: ensuring that outgoing commands can be generated reliably. Our results establish the utility of an emerging approach: understanding the structure of neural activity based on properties of population geometry that flow from normative principles such as noise robustness.