We use visual information to determine our dynamic relationship with other objects in a three-dimensional (3D) world. Despite decades of work on visual motion processing, it remains unclear how 3D directions-trajectories that include motion toward or away from the observer-are represented and processed in visual cortex. Area MT is heavily implicated in processing visual motion and depth, yet previous work has found little evidence for 3D direction sensitivity per se. Here we use a rich ensemble of binocular motion stimuli to reveal that most neurons in area MT of the anesthetized macaque encode 3D motion information. This tuning for 3D motion arises from multiple mechanisms, including different motion preferences in the two eyes and a nonlinear interaction of these signals when both eyes are stimulated. Using a novel method for functional binocular alignment, we were able to rule out contributions of static disparity tuning to the 3D motion tuning we observed. We propose that a primary function of MT is to encode 3D motion, critical for judging the movement of objects in dynamic real-world environments.
Although the visual system uses both velocity- and disparity-based binocular information for computing 3D motion, it is unknown whether (and how) these two signals interact. We found that these two binocular signals are processed distinctly at the levels of both cortical activity in human MT and perception. In human MT, adaptation to both velocity-based and disparity-based 3D motions demonstrated direction-selective neuroimaging responses. However, when adaptation to one cue was probed using the other cue, there was no evidence of interaction between them (i.e., there was no "cross-cue" adaptation). Analogous psychophysical measurements yielded correspondingly weak cross-cue motion aftereffects (MAEs) in the face of very strong within-cue adaptation. In a direct test of perceptual independence, adapting to opposite 3D directions generated by different binocular cues resulted in simultaneous, superimposed, opposite-direction MAEs. These findings suggest that velocity- and disparity-based 3D motion signals may both flow through area MT but constitute distinct signals and pathways.
Recently, T. B. Czuba, B. Rokers, K. Guillet, A. C. Huk, and L. K. Cormack, (2011) and Y. Sakano, R. S. Allison, and I. P. Howard (2012) published very similar studies using the motion aftereffect to probe the way in which motion through depth is computed. Here, we compare and contrast the findings of these two studies and incorporate their results with a brief follow-up experiment. Taken together, the results leave no doubt that the human visual system incorporates a mechanism that is uniquely sensitive to the difference in velocity signals between the two eyes, but--perhaps surprisingly--evidence for a neural representation of changes in binocular disparity over time remains elusive.
Motion aftereffects are historically considered evidence for neuronal populations tuned to specific directions of motion. Despite a wealth of motion aftereffect studies investigating 2D (frontoparallel) motion mechanisms, there is a remarkable dearth of psychophysical evidence for neuronal populations selective for the direction of motion through depth (i.e., tuned to 3D motion). We compared the effects of prolonged viewing of unidirectional motion under dichoptic and monocular conditions and found large 3D motion aftereffects that could not be explained by simple inheritance of 2D monocular aftereffects. These results (1) demonstrate the existence of neurons tuned to 3D motion as distinct from monocular 2D mechanisms, (2) show that distinct 3D direction selectivity arises from both interocular velocity differences and changing disparities over time, and (3) provide a straightforward psychophysical tool for further probing 3D motion mechanisms.
The movement of an object toward or away from the head is perhaps the most critical piece of information an organism can extract from its environment. Such 3D motion produces horizontally opposite motions on the two retinae. Little is known about how or where the visual system combines these two retinal motion signals, relative to the wealth of knowledge about the neural hierarchies involved in 2D motion processing and binocular vision. Canonical conceptions of primate visual processing assert that neurons early in the visual system combine monocular inputs into a single cyclopean stream (lacking eye-of-origin information) and extract 1D ("component") motions; later stages then extract 2D pattern motion from the cyclopean output of the earlier stage. Here, however, we show that 3D motion perception is in fact affected by the comparison of opposite 2D pattern motions between the two eyes. Three-dimensional motion sensitivity depends systematically on pattern motion direction when dichoptically viewing gratings and plaids-and a novel "dichoptic pseudoplaid" stimulus provides strong support for use of interocular pattern motion differences by precluding potential contributions from conventional disparity-based mechanisms. These results imply the existence of eye-of-origin information in later stages of motion processing and therefore motivate the incorporation of such eye-specific pattern-motion signals in models of motion processing and binocular integration.
Two binocular cues are thought to underlie the visual perception of three-dimensional (3D) motion: a disparity-based cue, which relies on changes in disparity over time, and a velocity-based cue, which relies on interocular velocity differences. The respective building blocks of these cues, instantaneous disparity and retinal motion, exhibit very distinct spatial and temporal signatures. Although these two cues are synchronous in naturally moving objects, disparity-based and velocity-based mechanisms can be dissociated experimentally. We therefore investigated how the relative contributions of these two cues change across a range of viewing conditions. We measured direction-discrimination sensitivity for motion though depth across a wide range of eccentricities and speeds for disparity-based stimuli, velocity-based stimuli, and "full cue" stimuli containing both changing disparities and interocular velocity differences. Surprisingly, the pattern of sensitivity for velocity-based stimuli was nearly identical to that for full cue stimuli across the entire extent of the measured spatiotemporal surface and both were clearly distinct from those for the disparity-based stimuli. These results suggest that for direction discrimination outside the fovea, 3D motion perception primarily relies on the velocity-based cue with little, if any, contribution from the disparity-based cue.