Transitions to and from microgravity, as experienced during a spaceflight mission, radically alter the demands on sensorimotor coordination. In this contribution, attention is directed to the vestibulo-oculomotor response to active head roll-tilt, generally referred to as ocular counterroll (OCR). Results are presented from a single-case longitudinal study over a 435-day spaceflight and from three further subjects over a 30-day period in microgravity. 1. Under one-g test conditions, with the head initially in the comfortable-upright position, active head-to-trunk roll tilt elicits a combined canal- and otolith-mediated oculomotor response, which manifests as a volley of torsional nystagmus beats combined with a tonic OCR. In microgravity it appears that only the transitory canal-mediated torsional nystagmus response remains. In both conditions the initial nystagmus response commences with an anticompensatory torsional fast phase. 2. Under zero-g conditions the head movements were comparable to those under one-g conditions but a consistent reduction in head velocity was observed. Despite this, eye velocity and eye-head velocity gain for the torsional component were found to be enhanced by up to 50% over the first thirty days in prolonged microgravity. 3. The results obtained from the 435-day mission indicate that the initially enhanced response decreases–over the course of several months–to preflight baseline level. The findings indicate that otolith- and canal-ocular responses are not simply added linearly, but rather that the afferent otolith signal also plays an inhibitory, or stabilising role on the canal-mediated response. Further, presuming a re-weighting of otolithic afferent information during prolonged microgravity, it is proposed that a corollary inverse re-weighting of corollary neck-proprioceptive afferences provides an effective substitute. In contrast to the idea that the torsional VOR is an evolutionary relic, it is postulated from the above findings that the anticompensatory saccade and the inherent low gain of OCR result as a compromise between intended reorientation to a tilted visual field and VOR compensation.