Detection of first- and second-order coherent motion in blindsight

Blindsight patients can detect fast moving stimuli presented within their blind field even when they deny any phenomenal visual experience. Although mounting evidence suggests the presence of different mechanisms and separate neural substrates underlying the processing of first-order (luminance-defined) and second-order (contrast-defined) motion, the perception of second-order motion in blindsight has scarcely been explored. In the present study, we investigated whether two blindsighted patients (GY and MS) can detect a variety of first- and second-order moving stimuli, and by using repetitive transcranial magnetic stimulation (rTMS), we assessed the role of V5/MT+ and V3+ in coherent motion processing. The hemianopes and four control subjects performed a two-interval forced-choice task in which they judged whether a pattern of coherently moving first-order or second-order textured squares moved in the first or second interval. They were not asked to report the direction of motion because neither of them could do so better than expected by chance. The results showed that MS, who has extensive destruction of the ventral cortical visual pathway as well as his V1 lesion, could not process second-order motion at all, whereas GY could perform second-order tasks but only at high-contrast modulation. This may have introduced first-order components in second-order moving stimuli and provided artifactual cues to motion. Moreover, rTMS delivered over area V5/MT+ impaired detection of both first- and second-order motion in undamaged control subjects, whereas rTMS over V3+ did not impair their performance in any of the stimuli employed. On the other hand, rTMS over V3+ did impair GY’s detection of first-order motion and high-contrast second-order moving textured squares that are likely to contain artifactual luminance cues. rTMS over V5/MT+ impaired first-order motion detection in MS. Overall, the results suggest that neither of the blindsight patients can detect artifact-free second-order motion.

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

[2]  L M Vaina,et al.  A lesion of cortical area V2 selectively impairs the perception of the direction of first‐order visual motion , 2000, Neuroreport.

[3]  H. Ashida,et al.  FMRI adaptation reveals separate mechanisms for first-order and second-order motion. , 2007, Journal of neurophysiology.

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

[5]  Alan Cowey,et al.  The cortical basis of global motion detection in blindsight , 2008, Experimental Brain Research.

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

[7]  G. Campana,et al.  Priming of first- and second-order motion: Mechanisms and neural substrates , 2008, Neuropsychologia.

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

[9]  Denis Schluppeck,et al.  Temporal characteristics of global motion processing revealed by transcranial magnetic stimulation , 2009, The European journal of neuroscience.

[10]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[11]  Alan Cowey,et al.  The neurobiology of blindsight , 1991, Trends in Neurosciences.

[12]  Lucia M Vaina,et al.  First-order and second-order motion: neurological evidence for neuroanatomically distinct systems. , 2004, Progress in brain research.

[13]  A. Cowey,et al.  The selective impairment of the perception of first-order motion by unilateral cortical brain damage , 1998, Visual Neuroscience.

[14]  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.

[15]  David A. Leopold,et al.  Blindsight depends on the lateral geniculate nucleus , 2010, Nature.

[16]  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.

[17]  Lucia M. Vaina,et al.  The role of human extra-striate visual areas V5/MT and V2/V3 in the perception of the direction of global motion: a transcranial magnetic stimulation study , 2006, Experimental Brain Research.

[18]  Timothy Ledgeway,et al.  Spatial frequency selective masking of first-order and second-order motion in the absence of off-frequency `looking' , 2004, Vision Research.

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

[20]  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.

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

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

[23]  Petra Stoerig,et al.  Blindsight, conscious vision, and the role of primary visual cortex. , 2006, Progress in brain research.

[24]  Isabelle Mareschal,et al.  A cortical locus for the processing of contrast-defined contours , 1998, Nature Neuroscience.

[25]  A. Cowey,et al.  Blindsight in man and monkey. , 1997, Brain : a journal of neurology.

[26]  C. Kennard,et al.  Residual colour vision in a human hemianope: spectral responses and colour discrimination , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[27]  C. Baker,et al.  Temporal and spatial response to second-order stimuli in cat area 18. , 1998, Journal of neurophysiology.

[28]  Sabrina Pitzalis,et al.  The cortical visual area V6 in macaque and human brains , 2009, Journal of Physiology-Paris.

[29]  A. Cowey.  The blindsight saga , 2009, Experimental Brain Research.

[30]  C. Baker.  Central neural mechanisms for detecting second-order motion , 1999, Current Opinion in Neurobiology.

[31]  C. Gross,et al.  Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  Mazyar Fallah,et al.  Response latencies of neurons in visual areas MT and MST of monkeys with striate cortex lesions , 2003, Neuropsychologia.

[33]  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.

[34]  M. Greenlee,et al.  The neuropsychology of vision , 2003 .

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

[36]  K H Ruddock,et al.  Human visual responses in the absence of the geniculo-calcarine projection. , 1980, Brain : a journal of neurology.

[37]  Svetlana S. Georgieva,et al.  The Processing of Three-Dimensional Shape from Disparity in the Human Brain , 2009, The Journal of Neuroscience.

[38]  G. Lennerstrand,et al.  AGE VARIATIONS IN NORMAL HUMAN CONTRAST SENSITIVITY , 1979, Acta ophthalmologica.

[39]  A. Cowey,et al.  Magnetically induced phosphenes in sighted, blind and blindsighted observers , 2000, Neuroreport.

[40]  Juha Silvanto,et al.  State-Dependency of Transcranial Magnetic Stimulation , 2008, Brain Topography.

[41]  A. Cowey.  Erratum to: The blindsight saga , 2010, Experimental Brain Research.

[42]  Paul B Hibbard,et al.  Consciousness of the first order in blindsight , 2010, Proceedings of the National Academy of Sciences.

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

[44]  Gianluca Campana,et al.  Priming of motion direction and area V5/MT: a test of perceptual memory. , 2002, Cerebral cortex.

[45]  L Weiskrantz,et al.  Visual capacity in the hemianopic field following a restricted occipital ablation. , 1974, Brain : a journal of neurology.

[46]  S Zeki,et al.  Conscious visual perception without V1. , 1993, Brain : a journal of neurology.

[47]  A. Cowey,et al.  Motion discrimination in cortically blind patients. , 2001, Brain : a journal of neurology.

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

[49]  Adriane E Seiffert,et al.  Functional MRI studies of human visual motion perception: texture, luminance, attention and after-effects. , 2003, Cerebral cortex.

[50]  H. Levitt.  Transformed up-down methods in psychoacoustics. , 1971, The Journal of the Acoustical Society of America.

[51]  Z. Cattaneo,et al.  Investigating visual motion perception using the transcranial magnetic stimulation-adaptation paradigm , 2008, Neuroreport.

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

[53]  C. Galletti,et al.  The cortical visual area V6: brain location and visual topography , 1999, The European journal of neuroscience.

[54]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

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

[56]  Chris J. Tinsley,et al.  Processing of first-order motion in marmoset visual cortex is influenced by second-order motion , 2006, Visual Neuroscience.

[57]  C. Galletti,et al.  The cortical connections of area V6: an occipito‐parietal network processing visual information , 2001, The European journal of neuroscience.

[58]  Juha Silvanto,et al.  Baseline cortical excitability determines whether TMS disrupts or facilitates behavior. , 2008, Journal of neurophysiology.

[59]  Saâd Jbabdi,et al.  Changes in connectivity after visual cortical brain damage underlie altered visual function. , 2008, Brain : a journal of neurology.

[60]  Z L Lu,et al.  Three-systems theory of human visual motion perception: review and update. , 2001, Journal of the Optical Society of America. A, Optics, image science, and vision.

[61]  C. E. Wright,et al.  The influence of age on the spatial and temporal contrast sensitivity function , 1985, Documenta Ophthalmologica.

[62]  C. Gross,et al.  Afferent basis of visual response properties in area MT of the macaque. II. Effects of superior colliculus removal , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[63]  N E Scott-Samuel,et al.  First-order and second-order signals combine to improve perceptual accuracy. , 2001, Journal of the Optical Society of America. A, Optics, image science, and vision.