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The retinal area inspecting a visual stimulus and, consequently, the number of photoreceptors engaged in a visual task increase with presentation time, as fixational eye movements continuously move the retina across the retinal image. Here, we varied stimulus duration in a Tumbling-E visual acuity task while recording videos of the photoreceptor mosaic in seven participants with adaptive optics micro-psychophysical techniques to determine how far the retinal image must move across the cone mosaic before this motion begins to improve visual acuity. Five stimulus presentation durations were tested (3, 80, 220, 370, and 600 ms), while participants exhibited natural eye movements. Retinal slip amplitudes (i.e., the total displacement stimuli underwent) increased linearly with stimulus duration at individual rates. Higher cone density was associated with drift over smaller retinal areas, making the number of traversed cones more similar across participants at longer durations. At the shortest presentation duration, retinal slip was virtually absent and acuity was limited by retinal resolution, averaging to 1.07 ± 0.08 times the cone row-to-row spacing (Nyquist limit of sampling). At an 80-ms duration, corresponding to approximately two cone diameters of retinal slip, acuity thresholds improved significantly, reaching 0.90 ± 0.10 of the Nyquist limit. Thresholds continued to improve with longer durations at a lower rate, reaching 0.75 ± 0.10 times the Nyquist limit at 600 ms. These results demonstrate that humans can extract visual information with sub-cone precision within less than 100 ms, with a retinal slip approaching single foveal cone spacing.