Estimating distance during self-motion: a role for visual-vestibular interactions.

A fundamental challenge for the visual system is to extract the 3D spatial structure of the environment. When an observer translates without moving the eyes, the retinal speed of a stationary object is related to its distance by a scale factor that depends on the velocity of the observer's self-motion. Here, we aim to test whether the brain uses vestibular cues to self-motion to estimate distance to stationary surfaces in the environment. This relationship was systematically probed using a two-alternative forced-choice task in which distance perceived from monocular image motion during passive body translation was compared to distance perceived from binocular disparity while subjects were stationary. We show that perceived distance from motion depended on both observer velocity and retinal speed. For a given head speed, slower retinal speeds led to the perception of farther distances. Likewise, for a given retinal speed, slower head speeds led to the perception of nearer distances. However, these relationships were weak in some subjects and absent in others, and distance estimated from self-motion and retinal image motion was substantially compressed relative to distance estimated from binocular disparity. Overall, our findings suggest that the combination of retinal image motion and vestibular signals related to head velocity can provide a rudimentary capacity for distance estimation.

[1]  W. Gogel,et al.  EQUIDISTANCE TENDENCY AND ITS CONSEQUENCES. , 1965, Psychological bulletin.

[2]  G. DeAngelis,et al.  A functional link between area MSTd and heading perception based on vestibular signals , 2007, Nature Neuroscience.

[3]  Mark Nawrot,et al.  The motion/pursuit law for visual depth perception from motion parallax , 2009, Vision Research.

[4]  E. Sture Eriksson.  Movement parallax during locomotion , 1974 .

[5]  K. Nakayama,et al.  Optical Velocity Patterns, Velocity-Sensitive Neurons, and Space Perception: A Hypothesis , 1974, Perception.

[6]  James A. Crowell,et al.  Horizontal and vertical disparity, eye position, and stereoscopic slant perception , 1999, Vision Research.

[7]  Hiroyasu Ujike,et al.  Motion Parallax Driven by Head Movements: Conditions for Visual Stability, Perceived Depth, and Perceived Concomitant Motion , 2005, Perception.

[8]  W. J. V. Damme,et al.  Non-visual Information in Structure-from-motion , 1996, Vision Research.

[9]  Herschel W. Leibowitz,et al.  Oculomotor adjustments in darkness and the specific distance tendency , 1976 .

[10]  Mark Nawrot,et al.  Eye movements provide the extra-retinal signal required for the perception of depth from motion parallax , 2003, Vision Research.

[11]  Lindsey Joyce,et al.  The pursuit theory of motion parallax , 2006, Vision Research.

[12]  John M. Foley,et al.  Primary Distance Perception , 1978 .

[13]  Dale Purves,et al.  A statistical explanation of visual space , 2003, Nature Neuroscience.

[14]  G. Johansson,et al.  Monocular Movement Parallax and Near-Space Perception , 1973 .

[15]  Bernhard J. M. Hess,et al.  Self-motion-induced eye movements: effects on visual acuity and navigation , 2005, Nature Reviews Neuroscience.

[16]  Fulvio Domini,et al.  Matching perceived depth from disparity and from velocity: Modeling and psychophysics. , 2010, Acta psychologica.

[17]  Dora E Angelaki,et al.  Does the Middle Temporal Area Carry Vestibular Signals Related to Self-Motion? , 2009, The Journal of Neuroscience.

[18]  J. Droulez,et al.  The visual perception of three-dimensional shape from self-motion and object-motion , 1994, Vision Research.

[19]  M. Banks,et al.  Estimator Reliability and Distance Scaling in Stereoscopic Slant Perception , 1999, Perception.

[20]  Heinrich H. Bülthoff,et al.  A Bayesian model of the disambiguation of gravitoinertial force by visual cues , 2007, Experimental Brain Research.

[21]  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.

[22]  M. Sanders.  Handbook of Sensory Physiology , 1975 .

[23]  Christopher R Fetsch,et al.  Dynamic Reweighting of Visual and Vestibular Cues during Self-Motion Perception , 2009, The Journal of Neuroscience.

[24]  Mark Nawrot,et al.  Depth from motion parallax scales with eye movement gain. , 2003, Journal of vision.

[25]  Dora E Angelaki,et al.  Visual and Nonvisual Contributions to Three-Dimensional Heading Selectivity in the Medial Superior Temporal Area , 2006, The Journal of Neuroscience.

[26]  Jack M. Loomis,et al.  Absolute motion parallax weakly determines visual scale in real and virtual environments , 1995, Electronic Imaging.

[27]  G. DeAngelis,et al.  Neural correlates of multisensory cue integration in macaque MSTd , 2008, Nature Neuroscience.

[28]  Mark Nawrot,et al.  MT Neurons Combine Visual Motion with a Smooth Eye Movement Signal to Code Depth-Sign from Motion Parallax , 2009, Neuron.

[29]  Jacques Droulez,et al.  Absolute distance perception during in-depth head movement: calibrating optic flow with extra-retinal information , 2002, Vision Research.

[30]  H. Ujike,et al.  Apparent Depth with Retinal Image Motion of Expansion and Contraction Yoked to Head Movement , 1998, Perception.

[31]  H. Ono,et al.  Apparent Depth with Motion Aftereffect and Head Movement , 1994, Perception.

[32]  M. Landy,et al.  Measurement and modeling of depth cue combination: in defense of weak fusion , 1995, Vision Research.

[33]  Jacques Droulez,et al.  Self-motion and the perception of stationary objects , 2001, Nature.

[34]  Gregory C. DeAngelis,et al.  A neural representation of depth from motion parallax in macaque visual cortex , 2008, Nature.

[35]  J. Droulez,et al.  Contribution of extraretinal signals to the scaling of object distance during self-motion , 2002, Perception & psychophysics.

[36]  Walter C. Gogel,et al.  A comparison of oculomotor and motion parallax cues of egocentric distance , 1979, Vision Research.

[37]  WALTER C. GOGEL,et al.  Absolute motion parallax and the specific distal 1 , 1973 .

[38]  B Rogers,et al.  Motion Parallax as an Independent Cue for Depth Perception , 1979, Perception.

[39]  R. Weale.  Vision. A Computational Investigation Into the Human Representation and Processing of Visual Information. David Marr , 1983 .

[40]  Gregory C DeAngelis,et al.  Coding of horizontal disparity and velocity by MT neurons in the alert macaque. , 2003, Journal of neurophysiology.

[41]  G P Bingham,et al.  The necessity of a perception-action approach to definite distance perception: monocular distance perception to guide reaching. , 1998, Journal of experimental psychology. Human perception and performance.

[42]  R. Wurtz,et al.  The role of disparity-sensitive cortical neurons in signalling the direction of self-motion , 1990, Nature.

[43]  J. Koenderink.  Optic flow , 1986, Vision Research.

[44]  J W Dees.  Accuracy of absolute visual distance and size estimation in space as a function of stereopsis and motion parallax. , 1966, Journal of experimental psychology.

[45]  G. DeAngelis,et al.  Fine Discrimination Training Alters the Causal Contribution of Macaque Area MT to Depth Perception , 2008, Neuron.

[46]  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.

[47]  Dora E Angelaki,et al.  Canal-otolith interactions and detection thresholds of linear and angular components during curved-path self-motion. , 2010, Journal of neurophysiology.

[48]  R. Hetherington.  The Perception of the Visual World , 1952 .

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

[50]  G. DeAngelis,et al.  Vestibular Heading Discrimination and Sensitivity to Linear Acceleration in Head and World Coordinates , 2010, The Journal of Neuroscience.

[51]  G. DeAngelis,et al.  Linking Neural Representation to Function in Stereoscopic Depth Perception: Roles of the Middle Temporal Area in Coarse versus Fine Disparity Discrimination , 2006, The Journal of Neuroscience.

[52]  James M. Hillis,et al.  Slant from texture and disparity cues: optimal cue combination. , 2004, Journal of vision.

[53]  S. H. Ferris.  Motion parallax and absolute distance. , 1972, Journal of experimental psychology.

[54]  M. Ernst,et al.  Focus cues affect perceived depth. , 2005, Journal of vision.

[55]  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.

[56]  C. Duffy,et al.  Heading representation in MST: sensory interactions and population encoding. , 2003, Journal of neurophysiology.