Dissociation in neuronal encoding of object versus surface motion in the primate brain

A paradox exists in our understanding of motion processing in the primate visual system: neurons in the dorsal motion processing stream often strikingly fail to encode long-range and perceptually salient jumps of a moving stimulus. Psychophysical studies suggest that such long-range motion, which requires integration over more distant parts of the visual field, may be based on higher-order motion processing mechanisms that rely on feature or object tracking. Here, we demonstrate that ventral visual area V4, long recognized as critical for processing static scenes, includes neurons that maintain direction selectivity for long-range motion, even when conflicting local motion is present. These V4 neurons exhibit specific selectivity for the motion of objects, i.e., targets with defined boundaries, rather than the motion of surfaces behind apertures, and are selective for direction of motion over a broad range of spatial displacements and defined by a variety of features. Motion direction at a range of speeds can be accurately decoded on single trials from the activity of just a few V4 neurons. Thus, our results identify a novel motion computation in the ventral stream that is strikingly different from, and complementary to, the well-established system in the dorsal stream, and they support the hypothesis that the ventral stream system interacts with the dorsal stream to achieve the higher level of abstraction critical for tracking dynamic objects.