Functional MRI studies of human visual motion perception: texture, luminance, attention and after-effects.

Motion of an object is thought to be perceived independently of the object's surface properties. However, theoretical, neuropsychological and psychophysical observations have suggested that motion of textures, called 'second-order motion', may be processed by a separate system from luminance-based, or 'first-order', motion. Functional magnetic resonance imaging (fMRI) responses during passive viewing, attentional modulation and post-adaptation motion after-effects (MAE) of these stimuli were measured in seven retinotopic visual areas (labeled V1, V2, V3, VP, V4v, V3A and LO) and the motion-sensitive area MT/MST (V5). In all visual areas, responses were strikingly similar to motion of first- and second-order stimuli. These results differ from a prior investigation, because here the motion-specific responses were isolated. Directing attention towards and away from the motion elicited equivalent response modulation for the two types. Dramatic post-adaptation (MAE) differences in perception of the two stimuli were observed and fMRI activation mimicked perceptual changes, but did not reveal the processing differences. In fact, no visual area was found to respond selectively to the motion of second-order stimuli, suggesting that motion perception arises from a unified motion detection system.

[1]  J M Zanker Second-order motion perception in the peripheral visual field. , 1997, Journal of the Optical Society of America. A, Optics, image science, and vision.

[2]  P. Cavanagh,et al.  Motion: the long and short of it. , 1989, Spatial vision.

[3]  T. Albright,et al.  Neuronal responses to edges defined by luminance vs. temporal texture in macaque area V1 , 1997, Visual Neuroscience.

[4]  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.

[5]  G. Sperling,et al.  The functional architecture of human visual motion perception , 1995, Vision Research.

[6]  C. Baker,et al.  Envelope-responsive neurons in areas 17 and 18 of cat. , 1994, Journal of neurophysiology.

[7]  M. Hershenson Linear and rotation motion aftereffects as a function of inspection duration , 1993, Vision Research.

[8]  J W Belliveau,et al.  Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. , 1995, Science.

[9]  T. Ledgeway Adaptation to second-order motion results in a motion aftereffect for directionally-ambiguous test stimuli , 1994, Vision Research.

[10]  A. T. Smith,et al.  Motion defined exclusively by second-order characteristics does not evoke optokinetic nystagmus , 1992, Visual Neuroscience.

[11]  F. Crick Function of the thalamic reticular complex: the searchlight hypothesis. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

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

[13]  R. Malach,et al.  Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[14]  S. Zeki Functional specialisation in the visual cortex of the rhesus monkey , 1978, Nature.

[15]  Ravi S. Menon,et al.  Recovery of fMRI activation in motion area MT following storage of the motion aftereffect. , 1999, Journal of neurophysiology.

[16]  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.

[17]  A. Johnston,et al.  Motion of contrast envelopes: peace and noise. , 2001, Journal of the Optical Society of America. A, Optics, image science, and vision.

[18]  H. Wilson,et al.  A psychophysically motivated model for two-dimensional motion perception , 1992, Visual Neuroscience.

[19]  D. Somers,et al.  Functional MRI reveals spatially specific attentional modulation in human primary visual cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[20]  H. J. Tochon-Danguy,et al.  Second Order Components of Moving Plaids Activate Extrastriate Cortex: A Positron Emission Tomography Study , 1999, NeuroImage.

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

[22]  G. Orban,et al.  A motion area in human visual cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[23]  A. Derrington,et al.  Second-order motion discrimination by feature-tracking , 1999, Vision Research.

[24]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[25]  P Cavanagh,et al.  Attention-based motion perception. , 1992, Science.

[26]  T. Hendler,et al.  Visuo-haptic object-related activation in the ventral visual pathway , 2001, Nature Neuroscience.

[27]  R. Tootell,et al.  Where is 'dorsal V4' in human visual cortex? Retinotopic, topographic and functional evidence. , 2001, Cerebral cortex.

[28]  P. Cavanagh,et al.  Position displacement, not velocity, is the cue to motion detection of second-order stimuli , 1998, Vision Research.

[29]  C. Furmanski,et al.  Selective Adaptation to Color Contrast in Human Primary Visual Cortex , 2001, The Journal of Neuroscience.

[30]  A J Ahumada,et al.  Model of human visual-motion sensing. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[31]  Stephen T. Hammett,et al.  Adaptation to motion of a second-order pattern: the motion aftereffect is not a general result , 1997, Vision Research.

[32]  A. Dale,et al.  Functional Analysis of V3A and Related Areas in Human Visual Cortex , 1997, The Journal of Neuroscience.

[33]  A. T. Smith,et al.  Detection and Discrimination of First- and Second-Order Motion in Patients with Unilateral Brain Damage , 1997, The Journal of Neuroscience.

[34]  A. Dale,et al.  The Representation of Illusory and Real Contours in Human Cortical Visual Areas Revealed by Functional Magnetic Resonance Imaging , 1999, The Journal of Neuroscience.

[35]  K. Grill-Spector,et al.  The dynamics of object-selective activation correlate with recognition performance in humans , 2000, Nature Neuroscience.

[36]  J. van Santen,et al.  Elaborated Reichardt detectors. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[37]  D. Heeger,et al.  Neuronal basis of contrast discrimination , 1999, Vision Research.

[38]  S. Hillyard,et al.  Involvement of striate and extrastriate visual cortical areas in spatial attention , 1999, Nature Neuroscience.

[39]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[40]  A. Cowey,et al.  Perception of first‐ and second‐order motion: Separable neurological mechanisms? , 1999, Human brain mapping.

[41]  E H Adelson,et al.  Spatiotemporal energy models for the perception of motion. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[42]  Leslie G. Ungerleider,et al.  Cue-dependent deficits in grating orientation discrimination after V4 lesions in macaques , 1996, Visual Neuroscience.

[43]  C L Baker,et al.  Spatial properties of envelope-responsive cells in area 17 and 18 neurons of the cat. , 1996, Journal of neurophysiology.

[44]  Kenneth I. Forster,et al.  Visual perception of rapidly presented word sequences of varying complexity , 1970 .

[45]  K. Nakayama,et al.  The characteristics of residual motion perception in the hemifield contralateral to lateral occipital lesions in humans. , 1993, Brain : a journal of neurology.

[46]  J. Hennig,et al.  The Processing of First- and Second-Order Motion in Human Visual Cortex Assessed by Functional Magnetic Resonance Imaging (fMRI) , 1998, The Journal of Neuroscience.

[47]  J J Knierim,et al.  Neural responses to visual texture patterns in middle temporal area of the macaque monkey. , 1992, Journal of neurophysiology.

[48]  N Osaka,et al.  Inefficient visual search for second-order motion. , 2001, Journal of the Optical Society of America. A, Optics, image science, and vision.

[49]  Barbara Anne Dosher,et al.  Attention mechanisms for multi-location first- and second-order motion perception , 2000, Vision Research.

[50]  I Mareschal,et al.  Cortical processing of second-order motion , 1999, Visual Neuroscience.

[51]  G. Sperling,et al.  Full-wave and half-wave rectification in second-order motion perception , 1994, Vision Research.

[52]  P. Cavanagh,et al.  Cortical fMRI activation produced by attentive tracking of moving targets. , 1998, Journal of neurophysiology.

[53]  Frans A. J. Verstraten,et al.  Visual motion and the human brain: what has neuroimaging told us? , 2001, Acta psychologica.

[54]  A. Cowey,et al.  Impairment of the perception of second order motion but not first order motion in a patient with unilateral focal brain damage , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[55]  A. T. Smith,et al.  Direction identification thresholds for second-order motion in central and peripheral vision. , 1994, Journal of the Optical Society of America. A, Optics, image science, and vision.

[56]  J. B. Demb,et al.  Cellular Basis for the Response to Second-Order Motion Cues in Y Retinal Ganglion Cells , 2001, Neuron.

[57]  C L Baker,et al.  A processing stream in mammalian visual cortex neurons for non-Fourier responses. , 1993, Science.

[58]  A. Johnston,et al.  A computational model of the analysis of some first-order and second-order motion patterns by simple and complex cells , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[59]  Talma Hendler,et al.  Center–periphery organization of human object areas , 2001, Nature Neuroscience.

[60]  A. Derrington,et al.  Motion of contrast-modulated gratings is analysed by different mechanisms at low and at high contrasts , 2000, Vision Research.

[61]  D. Heeger,et al.  Spatial attention affects brain activity in human primary visual cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[62]  S. Edelman,et al.  Cue-Invariant Activation in Object-Related Areas of the Human Occipital Lobe , 1998, Neuron.

[63]  A. Derrington,et al.  Separate detectors for simple and complex grating patterns? , 1985, Vision Research.

[64]  ANDREW T SMITH,et al.  Separate Detection of Moving Luminance and Contrast Modulations: Fact or Artifact? , 1997, Vision Research.

[65]  G. Orban,et al.  The kinetic occipital region in human visual cortex. , 1997, Cerebral cortex.

[66]  L. P. O'Keefe,et al.  Processing of first- and second-order motion signals by neurons in area MT of the macaque monkey , 1998, Visual Neuroscience.

[67]  D. Heeger,et al.  Neuronal Basis of the Motion Aftereffect Reconsidered , 2001, Neuron.

[68]  A. Johnston,et al.  Perceived motion of contrast-modulated gratings: Predictions of the multi-channel gradient model and the role of full-wave rectification , 1995, Vision Research.

[69]  G. Orban,et al.  The kinetic occipital (KO) region in man: an fMRI study. , 1997, Cerebral cortex.

[70]  P. Cavanagh,et al.  Position-based motion perception for color and texture stimuli: effects of contrast and speed , 1999, Vision Research.

[71]  G. Sperling,et al.  Drift-balanced random stimuli: a general basis for studying non-Fourier motion perception. , 1988, Journal of the Optical Society of America. A, Optics and image science.

[72]  T D Albright,et al.  Form-cue invariant motion processing in primate visual cortex. , 1992, Science.

[73]  Leslie G. Ungerleider,et al.  Texture segregation in the human visual cortex: A functional MRI study. , 2000, Journal of neurophysiology.

[74]  A. Pantle Immobility of some second-order stimuli in human peripheral vision. , 1992, Journal of the Optical Society of America. A, Optics and image science.