Thaddeus B. Czuba

Area MT Encodes Three-Dimensional Motion

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.

Three-dimensional motion aftereffects reveal distinct direction-selective mechanisms for binocular processing of motion through depth.

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.

To CD or not to CD: Is there a 3D motion aftereffect based on changing disparities?

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.

Binocular Mechanisms of 3D Motion Processing

The visual system must recover important properties of the external environment if its host is to survive. Because the retinae are effectively two-dimensional but the world is three-dimensional (3D), the patterns of stimulation both within and across the eyes must be used to infer the distal stimulus-the environment-in all three dimensions. Moreover, animals and elements in the environment move, which means the input contains rich temporal information. Here, in addition to reviewing the literature, we discuss how and why prior work has focused on purported isolated systems (e.g., stereopsis) or cues (e.g., horizontal disparity) that do not necessarily map elegantly on to the computations and complex patterns of stimulation that arise when visual systems operate within the real world. We thus also introduce the binoptic flow field (BFF) as a description of the 3D motion information available in realistic environments, which can foster the use of ecologically valid yet well-controlled stimuli. Further, it can help clarify how future studies can more directly focus on the computations and stimulus properties the visual system might use to support perception and behavior in a dynamic 3D world.

Separate Perceptual and Neural Processing of Velocity- and Disparity-Based 3D Motion Signals

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. SIGNIFICANCE STATEMENT Recent human neuroimaging and monkey electrophysiology have revealed 3D motion selectivity in area MT, which is driven by both velocity-based and disparity-based 3D motion signals. However, to elucidate the neural mechanisms by which the brain extracts 3D motion given these binocular signals, it is essential to understand how—or indeed if—these two binocular cues interact. We show that velocity-based and disparity-based signals are mostly separate at the levels of both fMRI responses in area MT and perception. Our findings suggest that the two binocular cues for 3D motion might be processed by separate specialized mechanisms.