Upper-limb movements are often composed of regular submovements, and neural correlates of submovement frequencies between 1 and 4 Hz have been found in the motor cortex. The temporal profile of movements is usually assumed to be determined by extrinsic factors such as limb biomechanics and feedback delays, but another possibility is that an intrinsic rhythmicity contributes to low frequencies in behavior. We used multielectrode recordings in monkeys performing an isometric movement task to reveal cyclic activity in primary motor cortex locked to submovements, and a distinct oscillation in premotor cortex. During ketamine sedation and natural sleep, cortical activity traversed similar cycles and became synchronized across areas. Because the same cortical dynamics are coupled to submovements and also observed in the absence of behavior, we conclude that the motor networks controlling the upper limb exhibit an intrinsic periodicity at submovement frequencies that is reflected in the speed profile of movements. •Local field potentials (LFPs) and neural firing are phase locked to submovements•Movement kinematics can be decoded from the areal velocity of LFP trajectories•The same dynamic patterns are seen during free reaching, sleep, and sedation•An intrinsic periodicity in motor circuits imposes temporal structure on behavior Hall et al. find that a common 3 Hz oscillation in the motor cortex of monkeys explains both the speed profile of movements and slow-wave activity during sleep and sedation. These results reveal how intrinsic network dynamics shape upper-limb behaviors.