Interaction of first- and second-order signals in the extraction of global-motion and optic-flow

The intention of this series of experiments was to determine the extent to which the pathways sensitive to first-order and second-order motion are independent of one another at, and above, the level of global motion integration. We used translational, radial and rotational motion stimuli containing luminance-modulated dots, contrast-modulated dots, or a mixture of both. Our results show that the two classes of motion stimuli interact perceptually in a global motion coherence task, and the extent of this interaction is governed by whether the two varieties of local motion signal produce an equivalent response in the pathways that encode each type of motion. This provides strong psychophysical evidence that global motion and optic flow processing are cue-invariant. The fidelity of the first-order motion signal was moderated by either reducing the luminance of the dots or by increasing the displacement of the dots on each positional update. The experiments were carried out with two different types of second-order elements (contrast-modulated dots and flicker-modulated dots) and the results were comparable, suggesting that these findings are generalisable to a variety of second-order stimuli. In addition, the interaction between the two different types of second-order stimuli was investigated and we found that the relative modulation depth was also crucial to whether the two populations interacted. We conclude that the relative output of local motion sensors sensitive to either first-order or second-order motion dictates their weight in subsequent cue-invariant global motion computations.

[1]  P. Cavanagh,et al.  Motion: the long and short of it. , 1989, Spatial vision.

[2]  John H. R. Maunsell,et al.  Visual processing in monkey extrastriate cortex. , 1987, Annual review of neuroscience.

[3]  T. Albright,et al.  Neuronal responses to edges defined by luminance vs. temporal texture in macaque area V1 , 1997, Visual Neuroscience.

[4]  D. Ringach,et al.  Topological analysis of population activity in visual cortex. , 2008, Journal of vision.

[5]  C. Baker,et al.  Residual motion perception in a "motion-blind" patient, assessed with limited-lifetime random dot stimuli , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  O. Braddick A short-range process in apparent motion. , 1974, Vision research.

[7]  T D Albright,et al.  Form-cue invariant motion processing in primate visual cortex. , 1992, Science.

[8]  Paul V McGraw,et al.  Deficits to global motion processing in human amblyopia , 2003, Vision Research.

[9]  G. Orban,et al.  The Speed Tuning of Medial Superior Temporal (Mst) Cell Responses to Optic-Flow Components , 1995, Perception.

[10]  R. Wurtz,et al.  Medial Superior Temporal Area Neurons Respond to Speed Patterns in Optic Flow , 1997, The Journal of Neuroscience.

[11]  K. H. Britten,et al.  Neuronal correlates of a perceptual decision , 1989, Nature.

[12]  Craig Aaen-Stockdale,et al.  Global motion processing: The effect of spatial scale and eccentricity. , 2008, Journal of vision.

[13]  Timothy Ledgeway,et al.  Spatial frequency selective masking of first-order and second-order motion in the absence of off-frequency `looking' , 2004, Vision Research.

[14]  J Zihl,et al.  The "motion-blind" patient: low-level spatial and temporal filters , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  U. Ilg,et al.  Processing of second-order motion stimuli in primate middle temporal area and medial superior temporal area. , 2001, Journal of the Optical Society of America. A, Optics, image science, and vision.

[16]  H. Wilson,et al.  A psychophysically motivated model for two-dimensional motion perception , 1992, Visual Neuroscience.

[17]  K. Tanaka,et al.  Analysis of motion of the visual field by direction, expansion/contraction, and rotation cells clustered in the dorsal part of the medial superior temporal area of the macaque monkey. , 1989, Journal of neurophysiology.

[18]  R A Andersen,et al.  The Analysis of Complex Motion Patterns by Form/Cue Invariant MSTd Neurons , 1996, The Journal of Neuroscience.

[19]  Temporal response properties to second-order visual stimuli in the LGN of cats , 2007 .

[20]  Z L Lu,et al.  Three-systems theory of human visual motion perception: review and update. , 2001, Journal of the Optical Society of America. A, Optics, image science, and vision.

[21]  D. Badcock,et al.  Global motion perception: No interaction between the first- and second-order motion pathways , 1995, Vision Research.

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

[23]  W. Newsome,et al.  Microstimulation in visual area MT: effects on direction discrimination performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[25]  Reza Farivar,et al.  Co-operative interactions between first- and second-order mechanisms in the processing of structure from motion. , 2010, Journal of vision.

[26]  Andrew T. Smith,et al.  Evidence for separate motion-detecting mechanisms for first- and second-order motion in human vision , 1994, Vision Research.

[27]  D. Regan,et al.  Looming detectors in the human visual pathway , 1978, Vision Research.

[28]  T. Albright,et al.  Motion coherency rules are form-cue invariant , 1992, Vision Research.

[29]  Ellen C. Hildreth,et al.  Measurement of Visual Motion , 1984 .

[30]  M. Georgeson,et al.  Does early non-linearity account for second-order motion? , 1999, Vision Research.

[31]  J A Perrone,et al.  Model for the computation of self-motion in biological systems. , 1992, Journal of the Optical Society of America. A, Optics and image science.

[32]  David R. Badcock,et al.  Detecting the displacement of periodic patterns , 1985, Vision Research.

[33]  G. Sperling,et al.  The functional architecture of human visual motion perception , 1995, Vision Research.

[34]  R. Allard,et al.  Double dissociation between first- and second-order processing , 2007, Vision Research.

[35]  B. Mansouri,et al.  The extent of the dorsal extra-striate deficit in amblyopia , 2006, Vision Research.

[36]  David R. Badcock,et al.  No interaction of first- and second-order signals in the extraction of global-motion and optic-flow , 2011, Vision Research.

[37]  J J Knierim,et al.  Neural responses to visual texture patterns in middle temporal area of the macaque monkey. , 1992, Journal of neurophysiology.

[38]  A. Leventhal,et al.  Neural correlates of boundary perception , 1998, Visual Neuroscience.

[39]  Craig Aaen-Stockdale,et al.  Biological motion perception is cue-invariant. , 2008, Journal of vision.

[40]  T. Ledgeway,et al.  Sensitivity to spatial and temporal modulations of first-order and second-order motion , 2006, Vision Research.

[41]  D R Badcock,et al.  Independent first- and second-order motion energy analyses of optic flow , 2001, Psychological research.

[42]  R. Hess,et al.  Investigating local network interactions underlying first- and second-order processing , 2004, Vision Research.

[43]  G. Sperling,et al.  Drift-balanced random stimuli: a general basis for studying non-Fourier motion perception. , 1988, Journal of the Optical Society of America. A, Optics and image science.

[44]  S. Nishida,et al.  Contrast Sensitivity of the Motion System , 1996, Vision Research.

[45]  S. Grossberg,et al.  A neural model of motion processing and visual navigation by cortical area MST. , 1999, Cerebral cortex.

[46]  W. Newsome,et al.  A selective impairment of motion perception following lesions of the middle temporal visual area (MT) , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  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.

[48]  Timothy Ledgeway,et al.  Second-order optic flow deficits in amblyopia. , 2007, Investigative ophthalmology & visual science.

[49]  C L Baker,et al.  A processing stream in mammalian visual cortex neurons for non-Fourier responses. , 1993, Science.

[50]  ANDREW T SMITH,et al.  Separate Detection of Moving Luminance and Contrast Modulations: Fact or Artifact? , 1997, Vision Research.

[51]  K. Tanaka,et al.  Underlying mechanisms of the response specificity of expansion/contraction and rotation cells in the dorsal part of the medial superior temporal area of the macaque monkey. , 1989, Journal of neurophysiology.

[52]  D. Burr,et al.  Temporal integration of optic flow, measured by contrast and coherence thresholds , 2001, Vision Research.

[53]  L. P. O'Keefe,et al.  Processing of first- and second-order motion signals by neurons in area MT of the macaque monkey , 1998, Visual Neuroscience.

[54]  T. Ledgeway,et al.  The influence of spatial and temporal noise on the detection of first-order and second-order orientation and motion direction , 2005, Vision Research.

[55]  Christopher Bowd,et al.  Direction discrimination of cyclopean (stereoscopic) and luminance motion , 1997, Vision Research.

[56]  C. Baker Central neural mechanisms for detecting second-order motion , 1999, Current Opinion in Neurobiology.

[57]  D Regan,et al.  Visual responses to vorticity and the neural analysis of optic flow. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[58]  Shin'ya Nishida,et al.  Dual multiple-scale processing for motion in the human visual System , 1997, Vision Research.

[59]  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.

[60]  A. Derrington,et al.  Separate detectors for simple and complex grating patterns? , 1985, Vision Research.

[61]  Vision Research , 1961, Nature.

[62]  Robert F. Hess,et al.  Second-order optic flow processing , 2007, Vision Research.

[63]  Keiji Tanaka,et al.  Integration of direction signals of image motion in the superior temporal sulcus of the macaque monkey , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.