Although originally examined in the context of prediction, it is now apparent that smooth eye movements generated by internal (extra-retinal) mechanisms play a role in both predictable and randomised pursuit responses. Internally generated responses are characterised by trajectories that begin with an increasing acceleration that develops much more slowly than responses generated through retinal feedback, but which can, nevertheless, reach high velocities. They can be evoked by regularly repeated motion stimuli or by cues that occur at a regular time before target motion onset. Although frequently observed as anticipatory movements, we now provide evidence that such movements also form the basis of the extra-retinal component of a randomised step-ramp response. In such circumstances they also build up slowly in the first second or so of the initial response. They are normally masked in the presence of visual feedback, but can be revealed by prolonged target extinction immediately after response initiation. The key to release internally generated responses in both random and predictable conditions is expectation of future target motion. The key to their functionality is rapid acquisition and storage of velocity and timing information.