The human cingulate sulcus visual area (CSv) responds selectively to visual and vestibular cues to self-motion. Although it is more selective for visual self-motion cues than any other brain region studied, it is not known whether CSv mediates perception of self-motion. An alternative hypothesis, based on its location, is that it provides sensory information to the motor system for use in guiding locomotion. To evaluate this hypothesis we studied the connectivity pattern of CSv, which is completely unknown, with a combination of diffusion MRI and resting-state functional MRI. Converging results from the 2 approaches suggest that visual drive is provided primarily by areas hV6, pVIP (putative intraparietal cortex) and PIC (posterior insular cortex). A strong connection with the medial portion of the somatosensory cortex, which represents the legs and feet, suggests that CSv may receive locomotion-relevant proprioceptive information as well as visual and vestibular signals. However, the dominant connections of CSv are with specific components of the motor system, in particular the cingulate motor areas and the supplementary motor area. We propose that CSv may provide a previously unknown link between perception and action that serves the online control of locomotion.