‘Real-motion’ cells in area V3A of macaque visual cortex

Summary

The stability of visual perception despite eye movements suggests the existence, in the visual system, of neural elements able to recognize whether a movement of an image occurring in a particular part of the retina is the consequence of an actual movement that occurred in the visual field, or self-induced by an ocular movement while the object was still in the field of view. Recordings from single neurons in area V3A of awake macaque monkeys were made to check the existence of such a type of neurons (called ‘real-motion’ cells; see Galletti et al. 1984, 1988) in this prestriate area of the visual cortex. A total of 119 neurons were recorded from area V3A. They were highly sensitive to the orientation of the visual stimuli, being on average more sensitive than V1 and V2 neurons. Almost all of them were sensitive to a large range of velocities of stimulus movement and about one half to the direction of it. In order to assess whether they gave different responses to the movement of a stimulus and to that of its retinal image alone (self-induced by an eye movement while the stimulus was still), a comparison was made between neuronal responses obtained when a moving stimulus swept a stationary receptive field (during steady fixation) and when a moving receptive field swept a stationary stimulus (during tracking eye movement). The receptive field stimulation at retinal level was physically the same in both cases, but only in the first was there actual movement of the visual stimulus. Control trials, where the monkeys performed tracking eye movements without any intentional receptive field stimulation, were also carried out. For a number of neurons, the test was repeated in darkness and against a textured visual background. Eighty-seven neurons were fully studied to assess whether they were real-motion cells. About 48% of them (42/87) showed significant differences between responses to stimulus versus eye movement. The great majority of these cells (36/42) were real-motion cells, in that they showed a weaker response to visual stimulation during tracking than to the actual stimulus movement during steady fixation. On average, the reduction in visual response during eye movement was 64.0 ± 15.7% (SD). Data obtained with a uniform visual background, together with those obtained in darkness and with textured background, indicate that real-motion cells receive an eye-motion input, either retinal or extraretinal in nature, probably acting presynaptically on the cell's visual input. In some cases, both retinal and extraretinal eye-motion inputs converge on the same real-motion cell. No correlation was observed between the real-motion behaviour and the sensitivity to either orientation or direction of movement of the visual stimulus used to activate the receptive field, nor with the retinotopic location of the receptive field. We suggest that the visual system uses real-motion cells in order to distinguish real from self-induced movements of retinal images, hence to recognize the actual movement in the visual field. Based on psychophysical data, the hypothesis has been advanced of an internal representation of the field of view, stable despite eye movement (cf. MacKay 1973). The real-motion cells may be neural elements of this network and we suggest that the visual system uses the output of this network to properly interpret the large number of sensory changes resulting from exploratory eye movements in a stable visual world.