Beyond Inheritance: De novo Fast Motion Computation in Primate Visual Cortex

Objects move through space and time, generating sequential visuotopic activations in all sighted animals leading to motion perception of velocity defined by direction and speed. Humans can effortlessly see motion with speeds ranging from 0.25 to 500°/s. However, direction-selective neurons in the primary visual cortex (V1)—from which all subsequent processing is presumed to derive— only encode directionality at low speeds. To resolve this paradox, we recorded neuronal responses to moving dots, gratings, and movies across the LGN, V1, MT and MST of the macaque motion pathway. Regardless of cell type and motion stimuli, V1 neurons lost direction selectivity at ∼29°/s while MT and MST neurons maintained it up to ∼82°/s and ∼183°/s, respectively. A cascaded spatiotemporal integration model reveals that at each cortex direction-selective neurons can generate velocity selectivity de novo, by integrating sequential visuotopic activations from preceding areas, irrespective of speed and directionality. By computing velocity anew, the primate brain effectively uses the cortical hierarchy itself to ‘shift gears’ to efficiently encode slow and fast motion. Thus, five visual areas from the retina into the brain’s processing hierarchy, external spatiotemporal information is being computed afresh, offering insights for motion processing in other species, modalities and machine vision.