Visual responses to contrast-defined contours with equally spatial-scaled carrier in cat area 18

Contrast-defined contours are one type of second-order contours, across which there are no differences in luminance. Although they can be always perceived, their responses have been only investigated when the spatial frequency of carrier, the background texture whose contrast is modulated to form contours, is much higher than that of contrast-defined contours, due to the interference of responses to luminance contours in other cases. In the present study, we examined visual responses in cat area 18 to the contrast-defined contours with carrier at same spatial frequency equal to neuron's preferred value for luminance contours, by establishing a control stimulus including all the luminance components but lack of the contrast contour information. Using single unit recording and intrinsic optical imaging, we demonstrated that contrast gratings with equally spatial-scaled carrier induced responses in a proportion of cat area 18 neurons with the preferred orientation similar to that for luminance contours, and the responses generated orientation maps similar to those for luminance contours. Our finding suggests that early visual cortex can process second-order contours regardless of the spatial frequency of carriers, in a way similar to the processing of luminance contours. This uniform manner of early visual processing might underlie the visual detection of both luminance contours and non-luminance second-order contours.

[1]  Amir Shmuel,et al.  The spatial pattern of response magnitude and selectivity for orientation and direction in cat visual cortex. , 2003, Cerebral cortex.

[2]  Sean P. MacEvoy,et al.  A precise form of divisive suppression supports population coding in primary visual cortex , 2009, Nature Neuroscience.

[3]  D. Burr,et al.  Functional implications of cross-orientation inhibition of cortical visual cells. I. Neurophysiological evidence , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[4]  C. Baker,et al.  Critical spatial frequencies for illusory contour processing in early visual cortex. , 2008, Cerebral cortex.

[5]  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.

[6]  L. Palmer,et al.  Retinotopic organization of areas 18 and 19 in the cat , 1979, The Journal of comparative neurology.

[7]  E. Adelson,et al.  The analysis of moving visual patterns , 1985 .

[8]  Chuan Yi Tang,et al.  A 2.|E|-Bit Distributed Algorithm for the Directed Euler Trail Problem , 1993, Inf. Process. Lett..

[9]  Baowang Li,et al.  Adaptation of PMLS neurons to prolonged optic flow stimuli , 2001, Neuroreport.

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

[11]  Temporal response properties to second-order visual stimuli in the LGN of cats , 2007 .

[12]  M. Seghier,et al.  Functional neuroimaging findings on the human perception of illusory contours , 2006, Neuroscience & Biobehavioral Reviews.

[13]  Y Matsuda,et al.  Arrangement of orientation pinwheel centers around area 17/18 transition zone in cat visual cortex. , 2000, Cerebral cortex.

[14]  Leonard E. White,et al.  Mapping multiple features in the population response of visual cortex , 2003, Nature.

[15]  Hiroki Tanaka,et al.  Neural Basis for Stereopsis from Second-Order Contrast Cues , 2006, The Journal of Neuroscience.

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

[17]  C. Baker,et al.  Processing of second-order stimuli in the visual cortex. , 2001, Progress in brain research.

[18]  Michael J. Hawken,et al.  Macaque VI neurons can signal ‘illusory’ contours , 1993, Nature.

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

[20]  Robert Shapley,et al.  Visual cortex: pushing the envelope , 1998, Nature Neuroscience.

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

[22]  E. Yund,et al.  Responses of striate cortex cells to grating and checkerboard patterns. , 1979, The Journal of physiology.

[23]  A. Nieder,et al.  Seeing more than meets the eye: processing of illusory contours in animals , 2002, Journal of Comparative Physiology A.

[24]  M. Sur,et al.  Orientation Maps of Subjective Contours in Visual Cortex , 1996, Science.

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

[26]  Curtis L Baker,et al.  Neural mechanisms mediating responses to abutting gratings: luminance edges vs. illusory contours. , 2006, Visual neuroscience.

[27]  N. Issa,et al.  Subcortical Representation of Non-Fourier Image Features , 2010, The Journal of Neuroscience.

[28]  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.

[29]  Dario L. Ringach,et al.  Dynamics of orientation tuning in macaque primary visual cortex , 1997, Nature.

[30]  Tiande Shou,et al.  The responses to illusory contours of neurons in cortex areas 17 and 18 of the cats , 2001, Science in China Series C: Life Sciences.

[31]  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.

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

[33]  R. von der Heydt,et al.  Illusory contours and cortical neuron responses. , 1984, Science.

[34]  Chang'an A Zhan,et al.  Boundary cue invariance in cortical orientation maps. , 2006, Cerebral cortex.

[35]  J. Movshon,et al.  Spatial summation in the receptive fields of simple cells in the cat's striate cortex. , 1978, The Journal of physiology.

[36]  C. Hung,et al.  Real and illusory contour processing in area V1 of the primate: a cortical balancing act. , 2001, Cerebral cortex.

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

[38]  I. Ohzawa,et al.  Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. II. Linearity of temporal and spatial summation. , 1993, Journal of neurophysiology.

[39]  R. von der Heydt,et al.  Mechanisms of contour perception in monkey visual cortex. I. Lines of pattern discontinuity , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  M. Carandini,et al.  Mapping of stimulus energy in primary visual cortex. , 2005, Journal of neurophysiology.

[41]  I. Ohzawa,et al.  Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. I. General characteristics and postnatal development. , 1993, Journal of neurophysiology.