Neural Trajectories in the Supplementary Motor Area and Motor Cortex Exhibit Distinct Geometries, Compatible with Different Classes of Computation

The supplementary motor area (SMA) is believed to contribute to higher order aspects of motor control. We considered a key higher order role: tracking progress throughout an action. We propose that doing so requires population activity to display low "trajectory divergence": situations with different future motor outputs should be distinct, even when present motor output is identical. We examined neural activity in SMA and primary motor cortex (M1) as monkeys cycled various distances through a virtual environment. SMA exhibited multiple response features that were absent in M1. At the single-neuron level, these included ramping firing rates and cycle-specific responses. At the population level, they included a helical population-trajectory geometry with shifts in the occupied subspace as movement unfolded. These diverse features all served to reduce trajectory divergence, which was much lower in SMA versus M1. Analogous population-trajectory geometry, also with low divergence, naturally arose in networks trained to internally guide multi-cycle movement. •Guiding action across time necessitates population activity with “low divergence”•The supplementary motor area, but not motor cortex, exhibits low divergence•Low divergence explains diverse single-neuron and population-level features The supplementary motor area is believed to guide action by “looking ahead” in time. Russo et al. formalize this idea and predict a basic property that neural activity must have to serve that purpose. That property is present, explains diverse features of activity, and distinguishes higher- from lower-level motor areas.