Motion signals in the visual field can cause strong biases in the perceived positions of stationary objects. Local motion signal within an object induces a shift in the perceived object position in the direction of motion, whereas adaptation to motion stimuli causes a perceptual shift in the opposite direction. The neural mechanisms underlying these illusions are poorly understood. Here we report two novel receptive field (RF) properties in cat primary visual cortex that may account for these motion-position illusions. First, motion signal in a stationary test stimulus causes a displacement of the RF in the direction opposite to motion. Second, motion adaptation induces a shift of the RF in the direction of adaptation. Comparison with human psychophysical measurements under similar conditions indicates that these RF properties can primarily account for the motion-position illusions. Importantly, both RF properties indicate a spatial asymmetry in the synaptic connections from direction-selective cells, and this circuit feature can be predicted by spike-timing-dependent synaptic plasticity, a widespread phenomenon in the nervous system. Thus, motion-induced perceptual mislocalization may be mediated by asymmetric cortical circuits, as a natural consequence of experience-dependent synaptic modification during circuit development.