Primary visual cortex neurons that contribute to resolve the aperture problem

It is traditional to believe that neurons in primary visual cortex are sensitive only or principally to stimulation within a spatially restricted receptive field (classical receptive field). It follows from this that they should only be capable of encoding the direction of stimulus movement orthogonal to the local contour, since this is the only information available in their classical receptive field “aperture.” This direction is not necessarily the same as the motion of the entire object, as the direction cue within an aperture is ambiguous to the global direction of motion, which can only be derived by integrating with unambiguous components of the object. Recent results, however, show that primary visual cortex neurons can integrate spatially and temporally distributed cues outside the classical receptive field, and so we reexamined whether primary visual cortex neurons suffer the “aperture problem.” With the stimulation of an optimally oriented bar drifting across the classical receptive field in different global directions, here we show that a subpopulation of primary visual cortex neurons (25/81) recorded from anesthetized and paralyzed marmosets is capable of integrating informative unambiguous direction cues presented by the bar ends, well outside their classical receptive fields, to encode global motion direction. Although the stimuli within the classical receptive field were identical, their directional responses were significantly modulated according to the global direction of stimulus movement. Hence, some primary visual cortex neurons are not local motion energy filters, but may encode signals that contribute directly to global motion processing.