Functional segregation of plural regions representing cardinal contours in cat primary visual cortex

Our previous data based on an imaging study suggested that, in cat area 17, the representations of cardinal orientations overlap less than the representation of their nearby angles. The purpose of this study was to further investigate the underlying single‐cell properties. Optical imaging was performed first to map the cortical regions corresponding to the four principal contours, the two cardinals and the two obliques. The cortical region activated by a principal orientation but not by the +10° or −10° neighbouring angles, namely the area with optically relative independent orientation selectivity (RIOS), was mapped together with the regions that overlapped with the +10° and/or −10° neighbouring angles (non‐RIOS). Electrode penetrations were targeted to the RIOS and non‐RIOS regions in each of the four orientations. A comparison between the RIOS and the non‐RIOS regions documented a significantly higher percentage of cells with the orientation preference of the cardinal orientations in the cardinal RIOS region than that seen in the other regions. Additionally, the difference in the tuning width of cells between the RIOS and non‐RIOS in the cardinal region was significantly larger than the difference between the RIOS and non‐RIOS in the oblique region. The cells in the cardinal RIOS region were tuned more sharply and the cells in cardinal non‐RIOS region more broadly than the oblique RIOS and/or the non‐RIOS region, which showed no significant difference. These data strongly suggest the existence of functional segregation in the region corresponding to the cardinal contours.

[1]  G. F. Cooper,et al.  The angular selectivity of visual cortical cells to moving gratings , 1968, The Journal of physiology.

[2]  Tobias Bonhoeffer,et al.  An Analysis of Orientation and Ocular Dominance Patterns in the Visual Cortex of Cats and Ferrets , 2000, Neural Computation.

[3]  M. Stryker,et al.  Development of Orientation Preference Maps in Ferret Primary Visual Cortex , 1996, The Journal of Neuroscience.

[4]  R. Bauer,et al.  Different anisotropies for texture and grating stimuli in the visual map of cat striate cortex , 1993, Vision Research.

[5]  K. Albus A quantitative study of the projection area of the central and the paracentral visual field in area 17 of the cat , 1975, Experimental brain research.

[6]  I. Ohzawa,et al.  Length and width tuning of neurons in the cat's primary visual cortex. , 1994, Journal of neurophysiology.

[7]  R. Freeman,et al.  Oblique effect: a neural basis in the visual cortex. , 2003, Journal of neurophysiology.

[8]  G A Orban,et al.  Preferences for horizontal or vertical orientation in cat visual cortical neurones [proceedings]. , 1979, The Journal of physiology.

[9]  R. Doty,et al.  Foveal striate cortex of behaving monkey: single-neuron responses to square-wave gratings during fixation of gaze. , 1977, Journal of neurophysiology.

[10]  R. L. Valois,et al.  The orientation and direction selectivity of cells in macaque visual cortex , 1982, Vision Research.

[11]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[12]  J. Movshon,et al.  Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons. , 2002, Journal of neurophysiology.

[13]  R. Shapley,et al.  Visual spatial characterization of macaque V1 neurons. , 2001, Journal of neurophysiology.

[14]  H. Ozeki,et al.  Relationship between Excitation and Inhibition Underlying Size Tuning and Contextual Response Modulation in the Cat Primary Visual Cortex , 2004, The Journal of Neuroscience.

[15]  Gang Wang,et al.  Representation of cardinal contour overlaps less with representation of nearby angles in cat visual cortex. , 2003, Journal of neurophysiology.

[16]  E. Hoffmann,et al.  Membrane potential, chloride exchange, and chloride conductance in Ehrlich mouse ascites tumour cells. , 1979, The Journal of physiology.

[17]  D. Fitzpatrick,et al.  Unequal representation of cardinal and oblique contours in ferret visual cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[18]  I. Ohzawa,et al.  Disinhibition Outside Receptive Fields in the Visual Cortex , 2002, The Journal of Neuroscience.

[19]  C. Blakemore,et al.  An analysis of orientation selectivity in the cat's visual cortex , 1974, Experimental Brain Research.

[20]  B R Payne,et al.  Functional organization of neurons in cat striate cortex: variations in preferred orientation and orientation selectivity with receptive-field type, ocular dominance, and location in visual-field map. , 1983, Journal of Neurophysiology.

[21]  T Bonhoeffer,et al.  Orientation selectivity in pinwheel centers in cat striate cortex. , 1997, Science.

[22]  S. Ronner,et al.  Orientation anisotropy in monkey visual cortex , 1978, Brain Research.

[23]  P. O. Bishop,et al.  Responses to moving slits by single units in cat striate cortex , 2004, Experimental Brain Research.

[24]  G. Orban,et al.  The influence of eccentricity on receptive field types and orientation selectivity in areas 17 and 18 of the cat , 1981, Brain Research.

[25]  T. Bonhoeffer,et al.  Overrepresentation of horizontal and vertical orientation preferences in developing ferret area 17. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[26]  B. Finlay,et al.  Meridional differences in orientation sensitivity in monkey striate cortex , 1976, Brain Research.

[27]  Amiram Grinvald,et al.  Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns , 1991, Nature.

[28]  D. Fitzpatrick,et al.  The contribution of sensory experience to the maturation of orientation selectivity in ferret visual cortex , 2001, Nature.

[29]  C. Gray,et al.  Heterogeneity in local distributions of orientation-selective neurons in the cat primary visual cortex , 1996, Visual Neuroscience.

[30]  H. Hirsch,et al.  Effects of early experience upon orientation sensitivity and binocularity of neurons in visual cortex of cats. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[31]  R. Mansfield,et al.  Neural Basis of Orientation Perception in Primate Vision , 1974, Science.

[32]  M. Sur,et al.  Optically imaged maps of orientation preference in primary visual cortex of cats and ferrets , 1997, The Journal of comparative neurology.

[33]  P. O. Bishop,et al.  Discrimination of orientation and position disparities by binocularly activated neurons in cat straite cortex. , 1977, Journal of neurophysiology.

[34]  Keiji Tanaka,et al.  Optical Imaging of Functional Organization in the Monkey Inferotemporal Cortex , 1996, Science.

[35]  Gang Wang,et al.  Difference in the representation of cardinal and oblique contours in cat visual cortex , 2003, Neuroscience Letters.

[36]  Keiji Tanaka,et al.  Effects of shape-discrimination training on the selectivity of inferotemporal cells in adult monkeys. , 1998, Journal of neurophysiology.

[37]  Keiji Tanaka,et al.  Functional architecture in monkey inferotemporal cortex revealed by in vivo optical imaging , 1998, Neuroscience Research.

[38]  M. Sur,et al.  Stability of Cortical Responses and the Statistics of Natural Scenes , 2001, Neuron.

[39]  G. Poggio,et al.  Binocular interaction and depth sensitivity in striate and prestriate cortex of behaving rhesus monkey. , 1977, Journal of neurophysiology.

[40]  A. Grinvald,et al.  A tandem-lens epifluorescence macroscope: Hundred-fold brightness advantage for wide-field imaging , 1991, Journal of Neuroscience Methods.