A unified model of heading and path perception in primate MSTd.

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.

Recurrent competition explains temporal effects of attention in MSTd.

Navigation in a static environment along straight paths without eye movements produces radial optic flow fields. A singularity called the focus of expansion (FoE) specifies the direction of travel (heading) of the observer. Cells in primate dorsal medial superior temporal area (MSTd) respond to radial fields and are therefore thought to be heading-sensitive. Humans frequently shift their focus of attention while navigating, for example, depending on the favorable or threatening context of approaching independently moving objects. Recent neurophysiological studies show that the spatial tuning curves of primate MSTd neurons change based on the difference in visual angle between an attentional prime and the FoE. Moreover, the peak mean population activity in MSTd retreats linearly in time as the distance between the attentional prime and FoE increases. We present a dynamical neural circuit model that demonstrates the same linear temporal peak shift observed electrophysiologically. The model qualitatively matches the neuron tuning curves and population activation profiles. After model MT dynamically pools short-range motion, model MSTd incorporates recurrent competition between units tuned to different radial optic flow templates, and integrates attentional signals from model area frontal eye fields (FEF). In the model, population activity peaks occur when the recurrent competition is most active and uncertainty is greatest about the relative position of the FoE. The nature of attention, multiplicative or non-multiplicative, is largely irrelevant, so long as attention has a Gaussian-like profile. Using an appropriately tuned sigmoidal signal function to modulate recurrent feedback affords qualitative fits of deflections in the population activity that otherwise appear to be low-frequency noise. We predict that these deflections mark changes in the balance of attention between the priming and FoE locations.

A neural circuit for robust time-to-contact estimation based on primate MST.

Time-to-contact (TTC) estimation is beneficial for visual navigation. It can be estimated from an image projection, either in a camera or on the retina, by looking at the rate of expansion of an object. When expansion rate (E) is properly defined, TTC = 1/E. Primate dorsal MST cells have receptive field structures suited to the estimation of expansion and TTC. However, the role of MST cells in TTC estimation has been discounted because of large receptive fields, the fact that neither they nor preceding brain areas appear to decompose the motion field to estimate divergence, and a lack of experimental data. This letter demonstrates mathematically that template models of dorsal MST cells can be constructed such that the output of the template match provides an accurate and robust estimate of TTC. The template match extracts the relevant components of the motion field and scales them such that the output of each component of the template match is an estimate of expansion. It then combines these component estimates to provide a mean estimate of expansion across the object. The output of model MST provides a direct measure of TTC. The ViSTARS model of primate visual navigation was updated to incorporate the modified templates. In ViSTARS and in primates, speed is represented as a population code in V1 and MT. A population code for speed complicates TTC estimation from a template match. Results presented in this letter demonstrate that the updated template model of MST accurately codes TTC across a population of model MST cells. We conclude that the updated template model of dorsal MST simultaneously and accurately codes TTC and heading regardless of receptive field size, object size, or motion representation. It is possible that a subpopulation of MST cells in primates represents expansion in this way.

A motion pooling model of visually guided navigation explains human behavior in the presence of independently moving objects.

Humans accurately judge their direction of heading when translating in a rigid environment, unless independently moving objects (IMOs) cross the observer's focus of expansion (FoE). Studies show that an IMO on a laterally moving path that maintains a fixed distance with respect to the observer (non-approaching; C. S. Royden & E. C. Hildreth, 1996) biases human heading estimates differently from an IMO on a lateral path that gets closer to the observer (approaching; W. H. Warren & J. A. Saunders, 1995). C. S. Royden (2002) argued that differential motion operators in primate brain area MT explained both data sets, concluding that differential motion was critical to human heading estimation. However, neurophysiological studies show that motion pooling cells, but not differential motion cells, in MT project to heading-sensitive cells in MST (V. K. Berezovskii & R. T. Born, 2000). It is difficult to reconcile differential motion heading models with these neurophysiological data. We generate motion sequences that mimic those viewed by human subjects. Model MT pools over V1; units in model MST perform distance-weighted template matching and compete in a recurrent heading representation layer. Our model produces heading biases of the same direction and magnitude as humans through a peak shift in model MSTd without using differential motion operators, maintaining consistency with known primate neurophysiology.

A neural model of how the brain computes heading from optic flow in realistic scenes.

Visually-based navigation is a key competence during spatial cognition. Animals avoid obstacles and approach goals in novel cluttered environments using optic flow to compute heading with respect to the environment. Most navigation models try either explain data, or to demonstrate navigational competence in real-world environments without regard to behavioral and neural substrates. The current article develops a model that does both. The ViSTARS neural model describes interactions among neurons in the primate magnocellular pathway, including V1, MT(+), and MSTd. Model outputs are quantitatively similar to human heading data in response to complex natural scenes. The model estimates heading to within 1.5 degrees in random dot or photo-realistically rendered scenes, and within 3 degrees in video streams from driving in real-world environments. Simulated rotations of less than 1 degrees /s do not affect heading estimates, but faster simulated rotation rates do, as in humans. The model is part of a larger navigational system that identifies and tracks objects while navigating in cluttered environments.