The distinction between eye and object motion is reflected by the motion-onset visual evoked potential

Humans are able to distinguish eye movement-induced retinal image motion and physical object motion during smooth pursuit eye movements. We investigated the neurophysiological basis of this ability by comparing motion-onset visual evoked potentials (VEPs) to onset of: (1) physical object motion during fixation, (2) eye movement-induced retinal image motion, and (3) physical object motion during eye movements. Electrooculographic (EOG) artifacts were removed and the influence of eye-movement quality was evaluated. Retinal image shift was of similar magnitude in all conditions (9°/s) and elicited typical motion-onset VEPs, with N2 at occipital and P2 at central derivations. During smooth pursuit, physical object motion induced N2 and P2 of higher latencies than during fixation. In the absence of physical object motion, i.e., for exclusively eye movement-induced retinal image motion, the N2 amplitude was reduced. This is taken as evidence that the activity of detectors of physical object motion is reflected by a part of the N2 component. N2 also reflects eye movement-induced retinal image motion. It is concluded that headcentric motion detection and the detection of eye movement-induced retinal image motion is mediated by brain mechanisms with similar latencies and, within the resolution limits of VEPs, at similar locations.

[1]  M. Bach,et al.  Stimulus versus eye movements: Comparison of neural activity in the striate and prelunate visual cortex (A17 and A19) of trained rhesus monkey , 2004, Experimental Brain Research.

[2]  Michael Bach,et al.  Directional tuning of human motion adaptation as reflected by the motion VEP , 2001, Vision Research.

[3]  Salvatore Squatrito,et al.  ‘Real-motion’ cells in the primary visual cortex of macaque monkeys , 1984, Brain Research.

[4]  P. Thier,et al.  Impaired analysis of moving objects due to deficient smooth pursuit eye movements. , 1999, Brain : a journal of neurology.

[5]  E. L. Keller,et al.  Smooth-pursuit initiation in the presence of a textured background in monkey , 1986, Vision Research.

[6]  F A Miles,et al.  Effects of stationary textured backgrounds on the initiation of pursuit eye movements in monkeys. , 1992, Journal of neurophysiology.

[7]  G. Glover,et al.  Retinotopic organization in human visual cortex and the spatial precision of functional MRI. , 1997, Cerebral cortex.

[8]  U. Ilg,et al.  Asymmetry in visual motion processing. , 1999, Neuroreport.

[9]  M. Kuba,et al.  Properties of visual evoked potentials to onset of movement on a television screen , 1990, Documenta Ophthalmologica.

[10]  VEP-Untersuchungen zur Kodierung der Geschwindigkeit bewegter Streifenmuster im Kortex des Menschen , 1985 .

[11]  U. Ilg Slow eye movements , 1997, Progress in Neurobiology.

[12]  Colin Blakemore,et al.  Contrast dependence of motion-onset and pattern-reversal evoked potentials , 1995, Vision Research.

[13]  R D Yee,et al.  Effects of an optokinetic background on pursuit eye movements. , 1983, Investigative ophthalmology & visual science.

[14]  P. Thier,et al.  Inability of Rhesus Monkey Area V1 to Discriminate Between Self‐induced and Externally Induced Retinal Image Slip , 1996, The European journal of neuroscience.

[15]  Frans A. J. Verstraten,et al.  The Motion Aftereffect:A Modern Perspective , 1998 .

[16]  J. Andreassi,et al.  Hemispheric sex differences in response to apparently moving stimuli as indicated by visual evoked potentials. , 1982, The International journal of neuroscience.

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

[18]  A. Dale,et al.  New images from human visual cortex , 1996, Trends in Neurosciences.

[19]  Joachim Mocks,et al.  Correcting ocular artifacts in the EEG: A comparison of several methods , 1989 .

[20]  W. Paulus,et al.  Identification of the visual motion area (area V5) in the human brain by dipole source analysis , 2004, Experimental Brain Research.

[21]  Michael Bach,et al.  Motion adaptation governs the shape of motion-evoked cortical potentials , 1994, Vision Research.

[22]  Peter Thier,et al.  An Electrophysiological Correlate of Visual Motion Awareness in Man , 1998, Journal of Cognitive Neuroscience.

[23]  M Niedeggen,et al.  Motion Aftereffects with Random-Dot Chequerboard Kinematograms: Relation between Psychophysical and VEP Measures , 1994, Perception.

[24]  E. Holst,et al.  Das Reafferenzprinzip , 2004, Naturwissenschaften.

[25]  B Bridgeman,et al.  Neither strong nor weak space constancy is coded in striate cortex , 1999, Psychological research.

[26]  D. Mackay,et al.  Electroencephalogram Potentials evoked by Accelerated Visual Motion , 1968, Nature.

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

[28]  S G Lisberger,et al.  Neuronal responses in visual areas MT and MST during smooth pursuit target selection. , 1997, Journal of neurophysiology.

[29]  G. Orban,et al.  Response latencies of visual cells in macaque areas V1, V2 and V5 , 1989, Brain Research.

[30]  C. Galletti,et al.  ‘Real-motion’ cells in visual area V2 of behaving macaque monkeys , 2004, Experimental Brain Research.

[31]  R. Sperry Neural basis of the spontaneous optokinetic response produced by visual inversion. , 1950, Journal of comparative and physiological psychology.

[32]  Alexander H. Wertheim,et al.  Motion perception during selfmotion: The direct versus inferential controversy revisited , 1994, Behavioral and Brain Sciences.

[33]  F. Markwardt,et al.  Influence of velocity, temporal frequency and initial phase position of grating patterns on motion VEP. , 1988, Biomedica biochimica acta.

[34]  P. Clarke,et al.  Visual evoked potentials to sudden reversal of the motion of a pattern. , 1972, Brain research.

[35]  P. Thier,et al.  A neuronal correlate of spatial stability during periods of self-induced visual motion , 2004, Experimental Brain Research.

[36]  A Puzzling Percept of Stimulus Stabilization , 1996, Vision Research.

[37]  Peter Thier,et al.  The influence of structured visual backgrounds on smooth-pursuit initiation, steady-state pursuit and smooth-pursuit termination , 1995, Biological Cybernetics.

[38]  P. Clarke,et al.  Comparison of visual evoked potentials to stationary and to moving patterns , 1973, Experimental Brain Research.

[39]  C. Tyler,et al.  Movement adaptation in the visual evoked response , 1977, Experimental Brain Research.

[40]  Isolation and characteristics of a steady-state visually-evoked potential in humans related to the motion of a stimulus , 1995, Vision Research.

[41]  R. Kleiser,et al.  Neural correlates of reafference: evoked brain activity during motion perception and saccadic eye movements , 2000, Experimental Brain Research.

[42]  H. Wässle,et al.  Response latency of brisk‐sustained (X) and brisk‐transient (Y) cells in the cat retina , 1982, The Journal of physiology.

[43]  Aya Takemura,et al.  Effects of smooth pursuit eye movement on ocular responses to sudden background motion in humans , 1999, Neuroscience Research.

[44]  R. Tootell,et al.  Anatomical evidence for MT and additional cortical visual areas in humans. , 1995, Cerebral cortex.

[45]  C. Galletti,et al.  ‘Real-motion’ cells in area V3A of macaque visual cortex , 2004, Experimental Brain Research.

[46]  J. Haxby,et al.  Functional anatomy of pursuit eye movements in humans as revealed by fMRI. , 1999, Journal of neurophysiology.

[47]  P. Clarke Visual evoked potentials to changes in the motion of a patterned field , 1973, Experimental Brain Research.

[48]  Michael Bach,et al.  Visual motion detection in man is governed by non-retinal mechanisms , 2000, Vision Research.

[49]  B W van Dijk,et al.  Motion-onset visual-evoked potentials as a function of retinal eccentricity in man. , 1993, Brain research. Cognitive brain research.

[50]  P. Clarke,et al.  Are visual evoked potentials to motion-reversal produced by direction-sensitive brain mechanisms? , 1974, Vision research.

[51]  Michael Bach,et al.  Contrast dependency of motion-onset and pattern-reversal VEPs: Interaction of stimulus type, recording site and response component , 1997, Vision Research.

[52]  R G Erickson,et al.  Responses of Direction‐Selective Neurons in Monkey Cortex to Self‐Induced Visual Motion , 1992, Annals of the New York Academy of Sciences.

[53]  Peter Thier,et al.  False perception of motion in a patient who cannot compensate for eye movements , 1997, Nature.

[54]  P. Thier,et al.  Responses of Visual‐Tracking Neurons from Cortical Area MST‐I to Visual, Eye and Head Motion , 1992, The European journal of neuroscience.

[55]  E. DeYoe,et al.  Mapping striate and extrastriate visual areas in human cerebral cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[56]  M. Goldberg,et al.  The visual and frontal cortices. , 1989, Reviews of oculomotor research.

[57]  Karl J. Friston,et al.  A direct demonstration of functional specialization in human visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  Peter Thier,et al.  Modification of the filehne illusion by conditioning visual stimuli , 1996, Vision Research.

[59]  Visuell evozierte Potentiale bei Musterbewegung , 1983 .

[60]  H. Jasper Report of the committee on methods of clinical examination in electroencephalography , 1958 .