Smooth pursuit eye movements have been described as resulting from the tracking of self-moved targets in total darkness. This study investigated the nature of the signal responsible for the release of smooth pursuit in this particular situation. Simultaneous monitoring of eye and hand positions shows that in total darkness smooth pursuit can only be released if the imagined target is either passively or actively moved by the subject's hand. An ischaemic block applied at the level of the biceps allowed us to selectively remove the afferent signal preferentially to the efferent copy in tasks involving eye tracking of an imaginary target actively or passively moved. The results show that an afferent signal was necessary and sufficient to release smooth pursuit, whereas the efferent copy alone could not trigger smooth pursuit. However, the efferent copy could play an important role in the phase relationship (prediction) between eye and finger events and in the activation of the concomitantly active saccadic system. Analysis of the eye movement characteristics, in various non-visually guided, load-affected situations, suggested that the main input to the smooth pursuit system was derived, in a non-graded way, from the position detector activation of the target-moving structure.