Mechanisms that allow cortical preparatory activity without inappropriate movement

We reveal a novel mechanism that explains how preparatory activity can evolve in motor-related cortical areas without prematurely inducing movement. The smooth eye movement region of the frontal eye fields (FEF(SEM)) is a critical node in the neural circuit controlling smooth pursuit eye movement. Preparatory activity evolves in the monkey FEF(SEM) during fixation in parallel with an objective measure of visual-motor gain. We propose that the use of FEF(SEM) output as a gain signal rather than a movement command allows for preparation to progress in pursuit without causing movement. We also show that preparatory modulation of firing rate in FEF(SEM) predicts movement, providing evidence against the ‘movement-null’ space hypothesis as an explanation of how preparatory activity can progress without movement. Finally, there is a partial reorganization of FEF(SEM) population activity between preparation and movement that would allow for a directionally non-specific component of preparatory visual-motor gain enhancement in pursuit.