A Unified Model of Heading and Path Perception in Primate MSTd

Author Summary Much human and primate psychological and electrophysiological research on visually-guided navigation has focused on heading perception, defined as the instantaneous direction of travel. However, the perception of path of travel, or trajectory, is arguably more important, because it informs in a more general sense whether the observer is on a collision course with moving objects or will intercept a target. In the present article, we describe a theory based on physiological evidence of how primate visual area MSTd may simultaneously and dynamically encode heading and path. The model connects many different sources of data, including psychophysics on human perception of heading and path with and without eye movements, and primate electrophysiological data on path-selective cells in MSTd. We propose neural mechanisms explaining why humans report traveling along curved paths when the display represents a straight path with simulated eye rotations. We predict that perceptual sensitivity to heading and path emerges in primate MSTd through the dynamical and competitive interactions between neurons tuned to the continuum of spiral-radial patterns. Self-motion, steering, and obstacle avoidance during navigation in the real world require humans to travel along curved paths. Many perceptual models have been proposed that focus on heading, which specifies the direction of travel along straight paths, but not on path curvature, which humans accurately perceive and is critical to everyday locomotion. In primates, including humans, dorsal medial superior temporal area (MSTd) has been implicated in heading perception. However, the majority of MSTd neurons respond optimally to spiral patterns, rather than to the radial expansion patterns associated with heading. No existing theory of curved path perception explains the neural mechanisms by which humans accurately assess path and no functional role for spiral-tuned cells has yet been proposed. Here we present a computational model that demonstrates how the continuum of observed cells (radial to circular) in MSTd can simultaneously code curvature and heading across the neural population. Curvature is encoded through the spirality of the most active cell, and heading is encoded through the visuotopic location of the center of the most active cell's receptive field. Model curvature and heading errors fit those made by humans. Our model challenges the view that the function of MSTd is heading estimation, based on our analysis we claim that it is primarily concerned with trajectory estimation and the simultaneous representation of both curvature and heading. In our model, temporal dynamics afford time-history in the neural representation of optic flow, which may modulate its structure. This has far-reaching implications for the interpretation of studies that assume that optic flow is, and should be, represented as an instantaneous vector field. Our results suggest that spiral motion patterns that emerge in spatio-temporal optic flow are essential for guiding self-motion along complex trajectories, and that cells in MSTd are specifically tuned to extract complex trajectory estimation from flow.