An Electrophysiological Correlate of Visual Motion Awareness in Man

It is usually held that perceptual spatial stability, despite smooth pursuit eye movements, is accomplished by comparing a signal reflecting retinal image slip with an internal reference signal, encoding the eye movement. The important consequence of this concept is that our subjective percept of visual motion reflects the outcome of this comparison rather than retinal image slip. In an attempt to localize the cortical networks underlying this comparison and therefore our subjective percept of visual motion, we exploited an imperfection inherent in it, which results in a movement illusion. If smooth pursuit is carried out across a stationary background, we perceive a tiny degree of illusionary background motion (Filehne illusion, or FI), rather than experiencing the ecologically optimal percept of stationarity. We have recently shown that this illusion can be modified substantially and predictably under laboratory conditions by visual motion unrelated to the eye movement. By making use of this finding, we were able to compare cortical potentials evoked by pursuit-induced retinal image slip under two conditions, which differed perceptually, while being identical physically. This approach allowed us to discern a pair of potentials, a parieto-occipital negativity (N300) followed by a frontal positivity (P300), whose amplitudes were solely determined by the subjective perception of visual motion irrespective of the physical attributes of the situation. This finding strongly suggests that subjective awareness of visual motion depends on neuronal activity in a parietooccipito-frontal network, which excludes the early stages of visual processing.

[1]  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.

[2]  B. Graaf,et al.  The perception of object motion during smooth pursuit eye movements: Adjacency is not a factor contributing to the filehne illusion , 1988, Vision Research.

[3]  A. Wertheim,et al.  Retinal and Extraretinal Information in Movement Perception: How to Invert the Filehne Illusion , 1987, Perception.

[4]  H. Komatsu,et al.  Relation of cortical areas MT and MST to pursuit eye movements. I. Localization and visual properties of neurons. , 1988, Journal of neurophysiology.

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

[6]  H. Komatsu,et al.  Relation of cortical areas MT and MST to pursuit eye movements. III. Interaction with full-field visual stimulation. , 1988, Journal of neurophysiology.

[7]  A. Dale,et al.  Visual motion aftereffect in human cortical area MT revealed by functional magnetic resonance imaging , 1995, Nature.

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

[9]  E Herman,et al.  Position Constancy during Pursuit Eye Movement: An Investigation of the Filehne Illusion , 1973, The Quarterly journal of experimental psychology.

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

[11]  Michael D. Rugg,et al.  Word and Nonword Repetition Within- and Across-Modality: An Event-Related Potential Study , 1995, Journal of Cognitive Neuroscience.

[12]  R. Andersen,et al.  Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  S. McKee,et al.  Statistical properties of forced-choice psychometric functions: Implications of probit analysis , 1985, Perception & psychophysics.

[14]  R Coppola,et al.  A new system for gray-level surface distribution maps of electrical activity. , 1982, Electroencephalography and clinical neurophysiology.

[15]  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.

[16]  A H Wertheim,et al.  On the relativity of perceived motion. , 1981, Acta psychologica.

[17]  K. Hoffmann,et al.  Responses of Neurons of the Nucleus of the Optic Tract and the Dorsal Terminal Nucleus of the Accessory Optic Tract in the Awake Monkey , 1996, The European journal of neuroscience.

[18]  H. B. Barlow,et al.  Visual illusion from running , 1996, Nature.

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

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

[21]  C. Koch,et al.  Are we aware of neural activity in primary visual cortex? , 1995, Nature.

[22]  M. M. Taylor,et al.  PEST: Efficient Estimates on Probability Functions , 1967 .

[23]  Edward Herman,et al.  The loss of position constancy during pursuit eye movements , 1978, Vision Research.