Faculty Bibliography

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.

How does the primate visual system encode three-dimensional motion? The macaque middle temporal area (MT) and the human MT complex (MT+) have well-established sensitivity to two-dimensional frontoparallel motion and static disparity. However, evidence for sensitivity to three-dimensional motion has remained elusive. We found that human MT+ encodes two binocular cues to three-dimensional motion: changing disparities over time and interocular comparisons of retinal velocities. By varying important properties of moving dot displays, we distinguished these three-dimensional motion signals from their constituents, instantaneous binocular disparity and monocular retinal motion. An adaptation experiment confirmed direction selectivity for three-dimensional motion. Our results indicate that MT+ carries critical binocular signals for three-dimensional motion processing, revealing an important and previously overlooked role for this well-studied brain area.

Popular hemodynamic brain imaging methods, such as blood oxygen-level dependent functional magnetic resonance imaging (BOLD fMRI), would benefit from a detailed understanding of the mechanisms by which oxygen is delivered to the cortex in response to brief periods of neural activity. Tissue oxygen responses in visual cortex following brief visual stimulation exhibit rich dynamics, including an early decrease in oxygen concentration, a subsequent large increase in concentration, and substantial late-time oscillations ("ringing"). We introduce a model that explains the full time-course of these observations made by Thompson et al. (2003). The model treats oxygen transport with a set of differential equations that include a combination of flow and diffusion in a three-compartment (intravascular, extravascular, and intracellular) system. Blood flow in this system is modeled using the impulse response of a lumped linear system that includes an inertive element; this provides a simple biophysical mechanism for the ringing. The model system is solved numerically to produce excellent fits to measurements of tissue oxygen. The results give insight into the dynamics of cerebral oxygen transfer, and can serve as the starting point to understand BOLD fMRI measurements.

Encoding the motion of objects through three spatial dimensions is a fundamental challenge for the visual system. Two binocular cues could contribute to the perception of motion through depth: changes in horizontal disparity (CD) and interocular velocity differences (IOVD). Although conceptually distinct, both cues are typically present when real objects move. Direct experimental isolation of the putative IOVD cue has remained elusive, and it is therefore unclear to what extent the visual system relies on it. We have found that binocularly anticorrelated stimuli impair position in depth judgments, but motion through depth judgments for the same stimuli are relatively unaffected. This dissociation of direction of motion from position in depth provides strong evidence that percepts of motion through depth are not based exclusively on estimating changes in disparity. Horizontal IOVDs appear to complement the CD cue. Vertical IOVDs fail to yield comparable performance, further implicating a comparison of horizontal interocular velocity and also ruling out explanations of our results based on monocular cues. These results suggest that (1) IOVDs are a robust cue to motion through depth; (2) IOVDs and retinal disparities exhibit similar horizontal/vertical anisotropies, consistent with the geometry of binocular viewing; and (3) binocular anticorrelation provides means to titrate the relative contributions of CD and IOVD cues.

An ellipse rotating in the image plane can produce several different percepts. The two-dimensional (2D) percepts are either a rotating rigid ellipse or a constantly deforming non-rigid ellipse. The 3D percept is a rotating rigid circular disk that is tilted relative to the image plane. Stimuli that generate 3D percepts based on purely 2D rotational motion are known as stereokinetic stimuli. We examined the 3D percepts generated by the rotating ellipse stimulus. In theory, the motion of the 3D percept cannot be reliably inferred based on the 2D stimulus. When we quantitatively estimated observers' perceived motion, however, we found that the perceived motion was nearly identical across observers. These results suggest that all observers had similar 3D percepts. We assumed that given the 2D rotating ellipse stimulus the visual system generates a rigid 3D percept that is as slow and smooth as possible. The percepts predicted by these assumptions closely matched the experimental data. These findings suggest that perceptual ambiguity in stereokinetic stimuli is resolved using slow and smooth motion assumptions.

Septohippocampal interactions determine how stimuli are encoded during conditioning. This study extends a previous neurocomputational model of corticohippocampal processing to incorporate hippocamposeptal feedback and examines how the presence or absence of such feedback affects learning in the model. The effects of septal modulation in conditioning were simulated by dynamically adjusting the hippocampal learning rate on the basis of how well the hippocampal system encoded stimuli. The model successfully accounts for changes in behavior and septohippocampal activity observed in studies of the acquisition, retention, and generalization of conditioned responses and accounts for the effects of septal disruption on conditioning. The model provides a computational, neurally based synthesis of prior learning theories that predicts changes in medial septal activity based on the novelty of stimulus events.