Using fMRI we wished to identify brain areas subserving the conversion of velocity signals into estimates of self-displacement (velocity-to-displacement integration, VDI), a function which is a prerequisite for the ability to navigate without landmarks. As real self-motion is not feasible in an fMRI environment, we presented subjects with a ride along a circular path in virtual reality devoid of usable landmarks. We asked subjects to try and feel as if actually moving in the scene and to either detect and count changes in driving speed (V-task) or to estimate the angular displacement achieved during a ride (D-task). We examined the contrast between these two tasks with regard to two hypothesised key functions for VDI: (1) evoking an internal image of the self in space and (2) manipulating this image in proportion to perceived velocity at the pace of a time base. The BOLD-responses during both tasks were fairly similar showing activity with right hemispheric dominance in a large parieto-temporo-occipital area as well as in frontal and prefrontal areas. Contrast D-V revealed a mainly parieto-hippocampal network comprising precuneus and inferior parietal cortex, posterior parieto-occipital cortex, retrosplenial cortex and the hippocampal region, but also right superior frontal gyrus and right cerebellum. It can be viewed as a blend of networks known to be involved in mental rotation and in navigation, except for the lack of ventral premotor and prefrontal activity. A tentative interpretation proposes a scenario where precuneus, together perhaps with posterior parieto-occipital cortex, provides the postulated mental image of the self in space and uses it to interpret results computed in the hippocampal region. In the hippocampal region, VDI proper would take place based on a map of spatial orientation, with the appropriate time scale being an intrinsic property. In addition, a dedicated time keeping system in inferior parietal cortex appears to be involved.