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.

[1]  W. Warren,et al.  The role of central and peripheral vision in perceiving the direction of self-motion , 1992, Perception & psychophysics.

[2]  Stephen Grossberg,et al.  Neural dynamics of motion integration and segmentation within and across apertures , 2001, Vision Research.

[3]  William H. Warren,et al.  Optic flow is used to control human walking , 2001, Nature Neuroscience.

[4]  Yong Gu,et al.  Decoding of MSTd Population Activity Accounts for Variations in the Precision of Heading Perception , 2010, Neuron.

[5]  B. Fajen,et al.  Perceiving curvilinear heading in the presence of moving objects. , 2002, Journal of experimental psychology. Human perception and performance.

[6]  James A. Crowell,et al.  Estimating heading during eye movements , 1994, Vision Research.

[7]  Constance S. Royden,et al.  Computing heading in the presence of moving objects: a model that uses motion-opponent operators , 2002, Vision Research.

[8]  C. Gross,et al.  Visual topography of striate projection zone (MT) in posterior superior temporal sulcus of the macaque. , 1981, Journal of neurophysiology.

[9]  Richard J. A. van Wezel,et al.  An illusory transformation of optic flow fields without local motion interactions , 2004, Vision Research.

[10]  G. Orban,et al.  Selectivity of Macaque MT/V5 Neurons for Surface Orientation in Depth Specified by Motion , 1997, The European journal of neuroscience.

[11]  Constance S. Royden,et al.  Differential effects of shared attention on perception of heading and 3-D object motion , 1999, Perception & psychophysics.

[12]  P Cavanagh,et al.  The Position of Moving Objects , 2000, Science.

[13]  Kenneth H. Britten,et al.  Mechanisms of self-motion perception. , 2008, Annual review of neuroscience.

[14]  Charles J. Duffy,et al.  Cortical neurons combine visual cues about self-movement , 2010, Experimental Brain Research.

[15]  Stephen Grossberg,et al.  Cortical dynamics of navigation and steering in natural scenes: Motion-based object segmentation, heading, and obstacle avoidance , 2009, Neural Networks.

[16]  Constance S. Royden,et al.  Modeling observer and object motion perception , 2004 .

[17]  S. Grossberg,et al.  Visual illusions in neural networks: line neutralization, tilt after effect, and angle expansion. , 1976, Journal of theoretical biology.

[18]  Constance S. Royden,et al.  Human heading judgments in the presence of moving objects , 1996, Perception & psychophysics.

[19]  Stephen Grossberg,et al.  A neural model of how the brain computes heading from optic flow in realistic scenes , 2009, Cognitive Psychology.

[20]  R. Wurtz,et al.  An illusory transformation of optic flow fields , 1993, Vision Research.

[21]  R. Wurtz,et al.  Sensitivity of MST neurons to optic flow stimuli. I. A continuum of response selectivity to large-field stimuli. , 1991, Journal of neurophysiology.

[22]  M. Lappe,et al.  The position of moving objects. , 2000, Perception.

[23]  S. Grossberg.  Contour Enhancement , Short Term Memory , and Constancies in Reverberating Neural Networks , 1973 .

[24]  G. Orban,et al.  Charting the Lower Superior Temporal Region, a New Motion-Sensitive Region in Monkey Superior Temporal Sulcus , 2006, The Journal of Neuroscience.

[25]  Guy A Orban,et al.  Higher order visual processing in macaque extrastriate cortex. , 2008, Physiological reviews.

[26]  Nicholas G. Hatsopoulos,et al.  On the sufficiency of the velocity field for perception of heading , 1991, Biological Cybernetics.

[27]  Diederick C Niehorster,et al.  A Bayesian model for estimating observer translation and rotation from optic flow and extra-retinal input. , 2010, Journal of vision.

[28]  David J Logan,et al.  Cerebral Cortex doi:10.1093/cercor/bhj082 Cerebral Cortex Advance Access published December 7, 2005 Cortical Area MSTd Combines Visual Cues , 2022 .

[29]  J. Gibson.  The Ecological Approach to Visual Perception , 1979 .

[30]  Richard J Krauzlis,et al.  Vector subtraction using visual and extraretinal motion signals: a new look at efference copy and corollary discharge theories. , 2008, Journal of vision.

[31]  Nicholas G. Hatsopoulos,et al.  Visual navigation with a neural network , 1991, Neural Networks.

[32]  S. Grossberg,et al.  Neural dynamics of motion processing and speed discrimination , 1998, Vision Research.

[33]  Constance S. Royden,et al.  Mathematical analysis of motion-opponent mechanisms used in the determination of heading and depth. , 1997, Journal of the Optical Society of America. A, Optics, image science, and vision.

[34]  Markus Lappe,et al.  A Neural Network for the Processing of Optic Flow from Ego-Motion in Man and Higher Mammals , 1993, Neural Computation.

[35]  D J Hannon,et al.  Eye movements and optical flow. , 1990, Journal of the Optical Society of America. A, Optics and image science.

[36]  H. C. Longuet-Higgins,et al.  The interpretation of a moving retinal image , 1980, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[37]  W. Warren,et al.  Perception of translational heading from optical flow. , 1988, Journal of experimental psychology. Human perception and performance.

[38]  Stephen Grossberg,et al.  Neural dynamics of motion grouping: from aperture ambiguity to object speed and direction , 1997 .

[39]  Constance S. Royden,et al.  A model using MT-like motion-opponent operators explains an illusory transformation in the optic flow field , 2003, Vision Research.

[40]  W. H. Warren.  The state of flow , 1998 .

[41]  Richard J A van Wezel,et al.  The role of motion capture in an illusory transformation of optic flow fields. , 2008, Journal of vision.

[42]  A. V. van den Berg,et al.  Heading detection using motion templates and eye velocity gain fields , 1998, Vision Research.

[43]  Ellen C. Hildreth,et al.  Recovering heading for visually-guided navigation , 1992, Vision Research.

[44]  Ennio Mingolla,et al.  Global induced motion and visual stability in an optic flow illusion , 1997, Vision Research.

[45]  D. Heeger.  Normalization of cell responses in cat striate cortex , 1992, Visual Neuroscience.

[46]  William H Warren,et al.  How do animals get about by vision? Visually controlled locomotion and orientation after 50 years. , 2009, British journal of psychology.

[47]  Leslie G. Ungerleider,et al.  Pathways for motion analysis: Cortical connections of the medial superior temporal and fundus of the superior temporal visual areas in the macaque , 1990, The Journal of comparative neurology.

[48]  Lawrence C. Sincich,et al.  The circuitry of V1 and V2: integration of color, form, and motion. , 2005, Annual review of neuroscience.

[49]  R. Wurtz,et al.  Response to motion in extrastriate area MSTl: center-surround interactions. , 1998, Journal of neurophysiology.

[50]  Christopher C. Pack,et al.  A Neural Model of Smooth Pursuit Control and Motion Perception by Cortical Area MST , 2001, Journal of Cognitive Neuroscience.

[51]  John H. R. Maunsell,et al.  The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  Nicholas J. Priebe,et al.  Comparison of the spatial limits on direction selectivity in visual areas MT and V1. , 2005, Journal of neurophysiology.

[53]  Heiko Neumann,et al.  A review and evaluation of methods estimating ego-motion , 2012, Comput. Vis. Image Underst..

[54]  R. Wurtz,et al.  Response of monkey MST neurons to optic flow stimuli with shifted centers of motion , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  Aijaz A. Baloch,et al.  A neural model of high-level motion processing: Line motion and formotion dynamics , 1997, Vision Research.

[56]  Navigation C. Hildreth.  Recovering Heading for Visually-Guided , 1992 .

[57]  Allan D. Jepson,et al.  Visual Perception of Three-Dimensional Motion , 1990, Neural Computation.

[58]  J H Rieger,et al.  Processing differential image motion. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[59]  E. Callaway,et al.  Multiple Circuits Relaying Primate Parallel Visual Pathways to the Middle Temporal Area , 2006, The Journal of Neuroscience.

[60]  Christopher C. Pack,et al.  Hierarchical processing of complex motion along the primate dorsal visual pathway , 2012, Proceedings of the National Academy of Sciences.

[61]  Stephen Grossberg,et al.  A neural model of visually guided steering, obstacle avoidance, and route selection. , 2009, Journal of experimental psychology. Human perception and performance.

[62]  J. Perrone,et al.  A model of self-motion estimation within primate extrastriate visual cortex , 1994, Vision Research.

[63]  R. Born,et al.  Specificity of Projections from Wide-Field and Local Motion-Processing Regions within the Middle Temporal Visual Area of the Owl Monkey , 2000, The Journal of Neuroscience.

[64]  A. P. Georgopoulos,et al.  Neuronal population coding of movement direction. , 1986, Science.

[65]  R. von der Heydt,et al.  Coding of Border Ownership in Monkey Visual Cortex , 2000, The Journal of Neuroscience.

[66]  R. Wurtz,et al.  Sensitivity of MST neurons to optic flow stimuli. II. Mechanisms of response selectivity revealed by small-field stimuli. , 1991, Journal of neurophysiology.

[67]  D. Bradley,et al.  Structure and function of visual area MT. , 2005, Annual review of neuroscience.

[68]  W H Warren,et al.  Perceiving Heading in the Presence of Moving Objects , 1995, Perception.