Visual pattern analysis relies on computations from neurons possessing spatially confined receptive fields. Often, such receptive fields are orders of magnitude larger than the visual pattern components being processed, as well as these components’ minute displacements on the retina, whether due to small object or self motions. Yet, perception effortlessly handles such visual conditions. Here, we show that in the primate superior colliculus, a brain structure long associated with oculomotor control, neurons with relatively large receptive fields are still sensitive to visual pattern displacements as small as 1 min arc. We used real-time gaze-contingent retinal image stabilization to control the instantaneous spatio-temporal luminance modulation of detailed patterns experienced by neurons, probing sensitivity to the lower limit of natural self-induced image displacements. Despite a large difference between pattern displacement amplitudes and receptive field sizes, collicular neurons were strongly sensitive to the visual pattern consequences of the smallest possible eye movements.