Microsaccades counteract perceptual filling-in.

Artificial scotomas positioned within peripheral dynamic noise fade perceptually during visual fixation (that is, the surrounding dynamic noise appears to fill-in the scotoma). Because the scotomas' edges are continuously refreshed by the dynamic noise background, this filling-in effect cannot be explained by low-level adaptation mechanisms (such as those that may underlie classical Troxler fading). We recently showed that microsaccades counteract Troxler fading and drive first-order visibility during fixation (S. Martinez-Conde, S. L. Macknik, X. G. Troncoso, & T. A. Dyar, 2006). Here we set out to determine whether microsaccades may counteract the perceptual filling-in of artificial scotomas and thus drive second-order visibility. If so, microsaccades may not only counteract low-level adaptation but also play a role in higher perceptual processes. We asked subjects to indicate, via button press/release, whether an artificial scotoma presented on a dynamic noise background was visible or invisible at any given time. The subjects' eye movements were simultaneously measured with a high precision video system. We found that increases in microsaccade production counteracted the perception of filling-in, driving the visibility of the artificial scotoma. Conversely, decreased microsaccades allowed perceptual filling-in to take place. Our results show that microsaccades do not solely overcome low-level adaptation mechanisms but they also contribute to maintaining second-order visibility during fixation.

[1]  R. L. Cohen,et al.  Adaptation effects and after effects of moving patterns viewed in the periphery of the visual field. , 1965, Scandinavian journal of psychology.

[2]  B. L. Zuber,et al.  Microsaccades and the Velocity-Amplitude Relationship for Saccadic Eye Movements , 1965, Science.

[3]  Ralf Engbert,et al.  Microsaccades Keep the Eyes' Balance During Fixation , 2004, Psychological science.

[4]  J. Krauskopf.  Effect of retinal image stabilization on the appearance of heterochromatic targets. , 1963, Journal of the Optical Society of America.

[5]  A. Safran.  Unperceived visual field defects. , 1997, Archives of ophthalmology.

[6]  S. Gielen,et al.  A quantitative analysis of generation of saccadic eye movements by burst neurons. , 1981, Journal of neurophysiology.

[7]  Ralf Engbert,et al.  Microsaccades uncover the orientation of covert attention , 2003, Vision Research.

[8]  Alejandro Lleras,et al.  Induced visual fading of complex images. , 2006, Journal of vision.

[9]  C. Evinger,et al.  Blinking and associated eye movements in humans, guinea pigs, and rabbits. , 1984, Journal of neurophysiology.

[10]  M. Sanders.  Control of Gaze by Brain Stem Neurons , 1978 .

[11]  R. L. Gregory,et al.  Perceptual filling in of artificially induced scotomas in human vision , 1991, Nature.

[12]  Xoana G. Troncoso,et al.  Saccades and microsaccades during visual fixation, exploration, and search: foundations for a common saccadic generator. , 2008, Journal of vision.

[13]  Janine D. Mendola,et al.  fMRI Measures of Perceptual Filling-in in the Human Visual Cortex , 2006 .

[14]  J. K. O'Regan.  No evidence for neural filling-in – vision as an illusion – pinning down “enaction” , 1998 .

[15]  D. Mackay,et al.  Anomalous Perception of Extrafoveal Motion , 1982, Perception.

[16]  Alejandro Lleras,et al.  What You See Is What You Get , 2006, Psychological science.

[17]  D. Hubel,et al.  The role of fixational eye movements in visual perception , 2004, Nature Reviews Neuroscience.

[18]  L. Dam,et al.  Retinal image shifts, but not eye movements per se, cause alternations in awareness during binocular rivalry , 2006 .

[19]  L. Spillmann,et al.  Filling-in of the foveal blue scotoma , 2001, Vision Research.

[20]  A. L. I︠A︡rbus.  Eye Movements and Vision , 1967 .

[21]  L. Pessoa,et al.  Filling-in: From perceptual completion to cortical reorganization. , 2003 .

[22]  S L Macknik,et al.  The role of spatiotemporal edges in visibility and visual masking. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[23]  F.J.J. Clarke,et al.  Visual Recovery Following Local Adaptation of the Peripheral Retina (Troxler's Effect) , 1961 .

[24]  P. de Weerd,et al.  Effects of Selective Attention on Perceptual Filling-in , 2006 .

[25]  Kai Hamburger,et al.  Perceptual filling-in from the edge of the blind spot , 2006, Vision Research.

[26]  H. Gerrits,et al.  The filling-in process in patients with retinal scotomata. , 1969, Vision research.

[27]  L. Spillmann,et al.  Flicker adaptation in the peripheral retina , 1987, Vision Research.

[28]  Shimon Ullman,et al.  Filling-in of retinal scotomas , 2003, Vision Research.

[29]  P. Blazquez,et al.  Kinematics of spontaneous, reflex, and conditioned eyelid movements in the alert cat. , 1995, Journal of neurophysiology.

[30]  F.J.J. Clarke,et al.  Rapid Light Adaptation of Localised Areas of the Extra-foveal Retina , 1957 .

[31]  Julie M. Harris,et al.  Filling-in the details on perceptual fading , 2001, Vision Research.

[32]  John S. Werner,et al.  Unveiling the foveal blue scotoma through an afterimage , 2004, Vision Research.

[33]  Peter De Weerd,et al.  Responses of cells in monkey visual cortex during perceptual filling-in of an artificial scotoma , 1995, Nature.

[34]  R. W. DITCHBURN,et al.  Vision with a Stabilized Retinal Image , 1952, Nature.

[35]  S. J. Belcher,et al.  On the localization of troxler's effect in the visual pathway , 1962 .

[36]  Leslie G. Ungerleider,et al.  Perceptual filling-in: a parametric study , 1998, Vision Research.

[37]  F. Møller,et al.  Binocular quantification and characterization of microsaccades , 2002, Graefe’s Archive for Clinical and Experimental Ophthalmology.

[38]  Ralf Engbert,et al.  Microsaccades are triggered by low retinal image slip. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[39]  D. Hubel,et al.  The function of bursts of spikes during visual fixation in the awake primate lateral geniculate nucleus and primary visual cortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[40]  S. Martinez-Conde.  Fixational eye movements in normal and pathological vision. , 2006, Progress in brain research.

[41]  G L WALLS,et al.  The filling-in process. , 1954, American journal of optometry and archives of American Academy of Optometry.

[42]  R. Kliegl,et al.  Shortening and prolongation of saccade latencies following microsaccades , 2006, Experimental Brain Research.

[43]  Reinhold Kliegl,et al.  Binocular coordination in microsaccades , 2003 .

[44]  C. Sharpe,et al.  The visibility and fading of thin lines visualized by their controlled movement across the retina , 1972, The Journal of physiology.

[45]  Peter De Weerd,et al.  Perceptual filling-in: More than the eye can see. , 2006, Progress in brain research.

[46]  Ralf Engbert,et al.  Toward a model of microsaccade generation: the case of microsaccadic inhibition. , 2008, Journal of vision.

[47]  F. Clarke.  A Study of Troxler's Effect , 1960 .

[48]  Ralf Engbert.  Microsaccades: A microcosm for research on oculomotor control, attention, and visual perception. , 2006, Progress in brain research.

[49]  Ralf Engbert,et al.  Microsaccade dynamics during covert attention , 2005, Vision Research.

[50]  L. Pessoa,et al.  Finding out about filling-in: a guide to perceptual completion for visual science and the philosophy of perception. , 1998, The Behavioral and brain sciences.

[51]  J. Alonso,et al.  Functional connectivity between simple cells and complex cells in cat striate cortex , 1998, Nature Neuroscience.

[52]  Vilayanur S. Ramachandran,et al.  Filling in: Why Dennett is wrong , 1993 .

[53]  A. L. Yarbus,et al.  Eye Movements and Vision , 1967, Springer US.

[54]  H. Gerrits,et al.  Simultaneous contrast, filling-in process and information processing in man's visual system , 1970, Experimental Brain Research.

[55]  H W Sabrin,et al.  The effect of imposed fixational eye movements on binocular rivalry , 1983, Perception & psychophysics.

[56]  Alex R. Wade,et al.  No Functional Magnetic Resonance Imaging Evidence for Brightness and Color Filling-In In Early Human Visual Cortex , 2006, The Journal of Neuroscience.

[57]  Vilayanur S. Ramachandran,et al.  Filling in: Why Dennett is wrong , 1993 .

[58]  Lothar Spillmann,et al.  Dynamic noise backgrounds facilitate target fading , 1992, Vision Research.

[59]  Lothar Spillmann,et al.  Texture fading correlates with stimulus salience , 2001, Vision Research.

[60]  J. Alonso,et al.  Construction of Complex Receptive Fields in Cat Primary Visual Cortex , 2001, Neuron.

[61]  Daniel C. Dennett.  Seeing is Believing--or is it? , 1996 .

[62]  Stephen L Macknik,et al.  Windows on the mind. , 2007, Scientific American.

[63]  D. Hubel,et al.  Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys , 2000, Nature Neuroscience.

[64]  Jay M. Enoch,et al.  Human psychophysical analysis of receptive field-like properties: V. Adaptation of stationary and moving windmill target characteristics to clinical populations , 1976, Documenta Ophthalmologica.

[65]  Catherine Hindi Attar,et al.  Uniform versus random orientation in fading and filling-in , 2007, Vision Research.

[66]  Xoana G. Troncoso,et al.  Microsaccades Counteract Visual Fading during Fixation , 2005, Neuron.

[67]  Peter De Weerd,et al.  Mechanisms of Surface Completion: Perceptual Filling-In of Texture , 2003 .

[68]  L. Spillmann,et al.  Movement adaptation in the peripheral retina , 1984, Vision Research.

[69]  Raymond van Ee,et al.  The role of (micro)saccades and blinks in perceptual bi-stability from slant rivalry , 2005, Vision Research.