Neurones in cat parastriate cortex sensitive to the direction of motion in three-dimensional space

1. On psychophysical grounds, Beverley & Regan suggested that in man different neural mechanisms mediate the binocular perception of movement in depth and the binocular perception of positional (static) depth. They proposed that the human visual pathway contains several neural mechanisms, each sensitive to a different direction of motion in space. These mechanisms compute the direction of motion from the relative speeds and directions of movement of the left and right retinal images.2. We have recorded from 101 units in area 18 of cat visual cortex, searching for neurones tuned to the direction of motion in three dimensions, with properties that could account for the proposed directionally tuned binocular motion detectors in man. The cat's left eye viewed one bar, while its right eye simultaneously viewed a second bar. Single units were stimulated by independently oscillating the bars from side to side. The apparent direction of movement in three dimensions was altered by varying the relative speeds of the bars and their relative directions of motion. The mean (positional) disparity of the bars could also be varied.3. For one class of neurone (twenty cells), binocular stimulation inhibited firing for trajectories parallel to the frontoparallel plane over a large volume of space. Strong firing was produced by oppositely directed bar movements. Some of these neurones were especially narrowly tuned to the direction of movement in depth, responding only to a range of 2-3 degrees , i.e. to moving bodies that would hit or only narrowly miss the cat. These cells emphasized the direction of movement at the expense of positional information.3. These units occurred in clusters. On the perpendicular penetrations in which they were found, they comprised a substantial majority of all cells encountered.5. For a second class of neurone (nine cells), binocular facilitation produced selective responses to objects moving along trajectories that missed the head.6. The two classes of neurone provide a basis for four proposed directionally tuned binocular motion detectors.7. A third class of neurone (seventeen cells) was selectively sensitive to movements parallel to the frontoparallel plane. There was strong binocular facilitation when the bars moved at the same speeds in the same directions: oppositely directed movements might be more than 100 times less effective. These neurones may signal positional disparity.8. These three classes of neurone cut across established categories. Only when both eyes were stimulated simultaneously with targets moving in different speeds and directions was it possible to demonstrate the binocular interactions described here.