Disparity-Based Coding of Three-Dimensional Surface Orientation by Macaque Middle Temporal Neurons

Gradients of binocular disparity across the visual field provide a potent cue to the three-dimensional (3-D) orientation of surfaces in a scene. Neurons selective for 3-D surface orientation defined by disparity gradients have recently been described in parietal cortex, but little is known about where and how this selectivity arises within the visual pathways. Because the middle temporal area (MT) has previously been implicated in depth perception, we tested whether MT neurons could signal the 3-D orientation (as parameterized by tilt and slant) of planar surfaces that were depicted by random-dot stereograms containing a linear gradient of horizontal disparities. We find that many MT neurons are tuned for 3-D surface orientation, and that tilt and slant generally have independent effects on MT responses. This separable coding of tilt and slant is reminiscent of the joint coding of variables in other areas (e.g., orientation and spatial frequency in V1). We show that tilt tuning remains unchanged when all coherent motion is removed from the visual stimuli, indicating that tilt selectivity is not a byproduct of 3-D velocity coding. Moreover, tilt tuning is typically insensitive to changes in the mean disparity (depth) of gradient stimuli, indicating that tilt tuning cannot be explained by conventional tuning for frontoparallel disparities. Finally, we explore the receptive field mechanisms underlying selectivity for 3-D surface orientation, and we show that tilt tuning arises through heterogeneous disparity tuning within the receptive fields of MT neurons. Our findings show that MT neurons carry high-level signals about 3-D surface structure, in addition to coding retinal image velocities.