Linear Summation of Repulsive and Attractive Serial Dependencies: Orientation and Motion Dependencies Sum in Motion Perception

Recent work from several groups has shown that perception of various visual attributes in human observers at a given moment is biased toward what was recently seen. This positive serial dependency is a kind of temporal averaging that exploits short-term correlations in visual scenes to reduce noise and stabilize perception. To date, this stabilizing “continuity field” has been demonstrated on stable visual attributes such as orientation and face identity, yet it would be counterproductive to apply it to dynamic attributes in which change sensitivity is needed. Here, we tested this using motion direction discrimination and predict a negative perceptual dependency: a contrastive relationship that enhances sensitivity to change. Surprisingly, our data showed a cubic-like pattern of dependencies with positive and negative components. By interleaving various stimulus combinations, we separated the components and isolated a positive perceptual dependency for motion and a negative dependency for orientation. A weighted linear sum of the separate dependencies described the original cubic pattern well. The positive dependency for motion shows an integrative perceptual effect and was unexpected, although it is consistent with work on motion priming. These findings suggest that a perception-stabilizing continuity field occurs pervasively, occurring even when it obscures sensitivity to dynamic stimuli. SIGNIFICANCE STATEMENT Recent studies show that visual perception at a given moment is not entirely veridical, but rather biased toward recently seen stimuli: a positive serial dependency. This temporal smoothing process helps perceptual continuity by preserving stable aspects of the visual scene over time, yet, for dynamic stimuli, temporal smoothing would blur dynamics and reduce sensitivity to change. We tested whether this process is selective for stable attributes by examining dependencies in motion perception. We found a clear positive dependency for motion, suggesting that positive perceptual dependencies are pervasive. We also found a concurrent negative (contrastive) dependency for orientation. Both dependencies combined linearly to determine perception, showing that the brain can calculate contrastive and integrative dependencies simultaneously from recent stimulus history when making perceptual decisions.

[1]  William A. Simpson,et al.  Temporal properties of the visual responses to luminance and contrast modulated noise , 2003, Vision Research.

[2]  Scott N. J. Watamaniuk,et al.  Temporal and spatial integration in dynamic random-dot stimuli , 1992, Vision Research.

[3]  D. G. Albrecht,et al.  Motion direction signals in the primary visual cortex of cat and monkey. , 2001, Visual neuroscience.

[4]  John Ross,et al.  Direct Evidence That “Speedlines” Influence Motion Mechanisms , 2002, The Journal of Neuroscience.

[5]  David C. Burr,et al.  The motion aftereffect of transparent motion: Two temporal channels account for perceived direction , 2005, Vision Research.

[6]  Duje Tadin,et al.  Perceptual and neural consequences of rapid motion adaptation , 2011, Proceedings of the National Academy of Sciences.

[7]  D. Alais,et al.  Orientation tuning of contrast masking caused by motion streaks. , 2010, Journal of vision.

[8]  M. Hershenson Duration, time constant, and decay of the linear motion aftereffect as a function of inspection duration , 1989, Perception & psychophysics.

[9]  David Alais,et al.  Motion streaks in fast motion rivalry cause orientation-selective suppression. , 2009, Journal of vision.

[10]  P. Wenderoth,et al.  The different mechanisms of the direct and indirect tilt illusions , 1988, Vision Research.

[11]  Floris P de Lange,et al.  Serial Dependence in Perceptual Decisions Is Reflected in Activity Patterns in Primary Visual Cortex , 2016, The Journal of Neuroscience.

[12]  D. Alais,et al.  Rapid Recalibration to Audiovisual Asynchrony , 2013, The Journal of Neuroscience.

[13]  F. D. Lange,et al.  Opposite Effects of Recent History on Perception and Decision , 2017, Current Biology.

[14]  J. Movshon,et al.  Adaptation changes the direction tuning of macaque MT neurons , 2004, Nature Neuroscience.

[15]  ROBERT FOX,et al.  Adaptation to invisible gratings and the site of binocular rivalry suppression , 1974, Nature.

[16]  David Badcock,et al.  The orientation dependence of the motion streak aftereffect reveals interactions between form and motion neurons. , 2015, Journal of vision.

[17]  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.

[18]  M. J. Morgan,et al.  Conditions for motion flow in dynamic visual noise , 1980, Vision Research.

[19]  D. Alais,et al.  The spatial tuning of "motion streak" mechanisms revealed by masking and adaptation. , 2011, Journal of vision.

[20]  Frans A. J. Verstraten,et al.  Perceptual manifestations of fast neural plasticity: Motion priming, rapid motion aftereffect and perceptual sensitization , 2005, Vision Research.

[21]  S. Suzuki Attention-dependent brief adaptation to contour orientation: a high-level aftereffect for convexity? , 2001, Vision Research.

[22]  J. Gibson,et al.  ADAPTATION , AFTEREFFECT AND CONTRAST IN THE PERCEPTION OF TILTED LINES , 2004 .

[23]  David Alais,et al.  Temporal Integration of Movement: The Time-Course of Motion Streaks Revealed by Masking , 2011, PloS one.

[24]  S. McKee,et al.  Sequential recruitment in the discrimination of velocity. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[25]  D. Burr,et al.  Compressive mapping of number to space reflects dynamic encoding mechanisms, not static logarithmic transform , 2014, Proceedings of the National Academy of Sciences.

[26]  David Alais,et al.  Audiovisual temporal recalibration occurs independently at two different time scales , 2015, Scientific Reports.

[27]  A. Pinkus,et al.  Probing Visual Motion Signals with a Priming Paradigm , 1997, Vision Research.

[28]  D. Whitney,et al.  Serial Dependence in the Perception of Faces , 2014, Current Biology.

[29]  D. Alais,et al.  Evidence for two interacting temporal channels in human visual processing , 2006, Vision Research.

[30]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[31]  David Alais,et al.  Different coding strategies for the perception of stable and changeable facial attributes , 2016, Scientific Reports.

[32]  C. Clifford Perceptual adaptation: motion parallels orientation , 2002, Trends in Cognitive Sciences.

[33]  J. Atick,et al.  STATISTICS OF NATURAL TIME-VARYING IMAGES , 1995 .

[34]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[35]  Leslie G. Ungerleider,et al.  Cortical connections of visual area MT in the macaque , 1986, The Journal of comparative neurology.

[36]  C. Cierpka,et al.  Particle imaging techniques for volumetric three-component (3D3C) velocity measurements in microfluidics , 2011, Journal of Visualization.

[37]  David C. Burr,et al.  Seeing biological motion , 1998, Nature.

[38]  G. Rhodes,et al.  How is facial expression coded? , 2015, Journal of vision.

[39]  Frans A. J. Verstraten,et al.  The motion aftereffect , 1998, Trends in Cognitive Sciences.

[40]  Michael Bach,et al.  Time course of motion adaptation: Motion-onset visual evoked potentials and subjective estimates , 1999, Vision Research.

[41]  N. Wade,et al.  The influence of colour and contour rivalry on the magnitude of the tilt after-effect , 1978, Vision Research.

[42]  Oliver Braddick,et al.  Interaction of spatial and temporal integration in global form processing , 2006, Vision Research.

[43]  Mark Edwards,et al.  Motion streaks improve motion detection , 2007, Vision Research.

[44]  D. Whitney,et al.  Serial dependence in visual perception , 2011 .

[45]  David R. Badcock,et al.  Rapidly acquired shape and face aftereffects are retinotopic and local in origin , 2012, Vision Research.

[46]  Mark W. Greenlee,et al.  Saturation of the tilt aftereffect , 1987, Vision Research.

[47]  Peter Wenderoth,et al.  The tilt illusion: Repulsion and attraction effects in the oblique meridian , 1977, Vision Research.

[48]  M. J. Keck,et al.  Recovery from Adaptation to Moving Gratings , 1977, Perception.

[49]  Eero P. Simoncelli,et al.  Local velocity representation: evidence from motion adaptation , 1998, Vision Research.

[50]  Justin M. Ales,et al.  The steady-state visual evoked potential in vision research: A review. , 2015, Journal of vision.

[51]  Wilson S. Geisler,et al.  Motion streaks provide a spatial code for motion direction , 1999, Nature.

[52]  David Alais,et al.  Rapid temporal recalibration occurs crossmodally without stimulus specificity but is absent unimodally , 2014, Brain Research.

[53]  D. Samuel Schwarzkopf,et al.  Direct evidence for encoding of motion streaks in human visual cortex , 2013, Proceedings of the Royal Society B: Biological Sciences.

[54]  D. Alais,et al.  Tilt aftereffects and tilt illusions induced by fast translational motion: evidence for motion streaks. , 2009, Journal of vision.

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

[56]  R. Sekuler,et al.  Adaptation alters perceived direction of motion , 1976, Vision Research.

[57]  D. Alais,et al.  Love at second sight: Sequential dependence of facial attractiveness in an on-line dating paradigm , 2016, Scientific Reports.

[58]  Matthew F. Tang,et al.  The broad orientation dependence of the motion streak aftereffect reveals interactions between form and motion neurons. , 2015, Journal of vision.

[59]  C. Clifford,et al.  A functional angle on some after-effects in cortical vision , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[60]  O J Braddick,et al.  Temporal Properties of the Short-Range Process in Apparent Motion , 1985, Perception.

[61]  O. Braddick,et al.  The temporal integration and resolution of velocity signals , 1991, Vision Research.

[62]  R Sekuler,et al.  Letter: Tilt aftereffect following very brief exposures. , 1974, Vision research.

[63]  D. Burr Temporal summation of moving images by the human visual system , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[64]  David Alais,et al.  Auditory frequency perception adapts rapidly to the immediate past , 2015, Attention, perception & psychophysics.