Separate visual representations for perception and action revealed by saccadic eye movements

Some 30 years ago, Trevarthen [1] introduced the idea of two separate visual systems, a focal system for fine motor acts and an ambient system for gross body movements such as ambulation. More recent developments indicating anatomically and physiologically separate pathways in primate vision [2] have led to a different idea of separate visual systems, one for conscious perception and one for action [3]. It has received empirical support from several studies showing that pointing, reaching, and grasping can remain accurate while the perceived position or size of objects is subject to illusory distortion [4-6]. However, much of this evidence has been challenged on the grounds of methodological flaws, particularly failure to match perfectly the conditions for verbal and motor tasks and failure to replicate results [7-10]. Here we take advantage of the strong compression of perceived position that occurs around the time of saccadic eye movements [11, 12]. Under normal lighting conditions, stimuli flashed briefly over a wide range of spatial positions just before saccadic onset are neither seen nor reached for in their veridical positions, but are compressed toward the saccadic target. We validate the idea of separate systems by showing that, in the dark, subjects are able to point accurately to the correct target position, even though their verbal reports are still subject to compression.

[1]  David C. Burr,et al.  Compression of visual space before saccades , 1997, Nature.

[2]  P Dassonville,et al.  Oculomotor localization relies on a damped representation of saccadic eye displacement in human and nonhuman primates , 1992, Visual Neuroscience.

[3]  H. Bülthoff,et al.  Separate neural pathways for the visual analysis of object shape in perception and prehension , 1994, Current Biology.

[4]  R. Andersen,et al.  Models of the Posterior Parietal Cortex Which Perform Multimodal Integration and Represent Space in Several Coordinate Frames , 2000, Journal of Cognitive Neuroscience.

[5]  J R Duhamel,et al.  The updating of the representation of visual space in parietal cortex by intended eye movements. , 1992, Science.

[6]  B. Bridgeman,et al.  Postsaccadic target blanking prevents saccadic suppression of image displacement , 1996, Vision Research.

[7]  Bruce Bridgeman,et al.  Failure to detect displacement of the visual world during saccadic eye movements , 1975, Vision Research.

[8]  M. Goldberg,et al.  Neurons in the monkey superior colliculus predict the visual result of impending saccadic eye movements. , 1995, Journal of neurophysiology.

[9]  M. Goodale,et al.  Size-contrast illusions deceive the eye but not the hand , 1995, Current Biology.

[10]  L. Matin Eye Movements and Perceived Visual Direction , 1972 .

[11]  Alexandre Pouget,et al.  Perceived geometrical relationships affected by eye-movement signals , 1997, Nature.

[12]  M. Concetta Morrone,et al.  Apparent Position of Visual Targets during Real and Simulated Saccadic Eye Movements , 1997, The Journal of Neuroscience.

[13]  Ronald M. Hansen,et al.  Accuracy of spatial localizations near the time of saccadic eye movements , 1985, Vision Research.

[14]  H. Honda Perceptual localization of visual stimuli flashed during saccades , 1989, Perception & psychophysics.

[15]  C. Trevarthen,et al.  Two mechanisms of vision in primates , 1968, Psychologische Forschung.

[16]  B. Bridgeman,et al.  Immediate post-saccadic information mediates space constancy , 1998, Vision Research.

[17]  P. E. Hallett,et al.  Saccadic eye movements to flashed targets , 1976, Vision Research.

[18]  Christopher J Bockisch,et al.  Different motor systems use similar damped extraretinal eye position information , 1999, Vision Research.

[19]  F. Bremmer,et al.  Spatial invariance of visual receptive fields in parietal cortex neurons , 1997, Nature.

[20]  Masud Husain,et al.  Reaching movements may reveal the distorted topography of spatial representations after neglect , 2000, Neuropsychologia.

[21]  Richard A. Andersen,et al.  Separate body- and world-referenced representations of visual space in parietal cortex , 1998, Nature.

[22]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[23]  Paul Dassonville,et al.  The use of egocentric and exocentric location cues in saccadic programming , 1995, Vision Research.

[24]  M. Fahle,et al.  Grasping Visual Illusions: No Evidence for a Dissociation Between Perception and Action , 2000, Psychological science.

[25]  Leslie G. Ungerleider,et al.  Object vision and spatial vision: two cortical pathways , 1983, Trends in Neurosciences.

[26]  C. Galletti,et al.  Eye Position Influence on the Parieto‐occipital Area PO (V6) of the Macaque Monkey , 1995, The European journal of neuroscience.

[27]  Bart Krekelberg,et al.  Postsaccadic visual references generate presaccadic compression of space , 2000, Nature.