Topographic relations between ocular dominance and orientation columns in the cat striate cortex

SummaryIn the visual cortex of four adult cats ocular dominance and orientation columns were visualized with (3H)proline and (14C)deoxyglucose autoradiography. The two columnar systems were reconstructed from serial horizontal sections or from flat-mount preparations and graphically superimposed. They share a number of characteristic features: In both systems the columns have a tendency to form regularly spaced parallel bands whose main trajectory is perpendicular to the border between areas 17 and 18. These bands frequently bifurcate or terminate in blind endings. The resulting irregularities are much more pronounced in the ocular dominance than in the orientation system. The periodicity of the columnar patterns was assessed along trajectories perpendicular to the main orientation of the bands and differed in the two columnar systems. The spacing of the ocular dominance stripes was significantly narrower than the spacing of orientation bands. The mean periodicity of a particular columnar system was virtually identical in the two hemispheres of the same animal but it differed substantially in different animals. However, the spacing of orientation columns covaried with that of the ocular dominance columns, the ratios of the mean spacings of the two columnar systems being similar in the four cats. The superposition of the two columnar systems revealed no obvious topographic relation between any of the organizational details such as the location of bifurcations, blind endings and intersections. We suggest the following conclusions: 1. The developmental processes generating the two columnar systems seem to obey the same algorithms but they act independently of each other. 2. The space constants of the two systems are rigorously specified and appear to depend on a common variable. 3. The main orientation of the bands in both columnar systems is related to a) the representation of the vertical meridian, b) the anisotropy of the cortical magnification factor, and c) the tangential spread of intracortical connections.

[1]  M. Stryker,et al.  Physiological evidence that the 2-deoxyglucose method reveals orientation columns in cat visual cortex , 1981, Nature.

[2]  O. Creutzfeldt,et al.  The distribution of degenerating axons after small lesions in the intact and isolated visual cortex of the cat , 1977, Experimental Brain Research.

[3]  A. L. Humphrey,et al.  Topographic organization of the orientation column system in the striate cortex of the tree shrew (Tupaia glis). I. Microelectrode recording , 1980, The Journal of comparative neurology.

[4]  D. Hubel,et al.  Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey , 1981, Nature.

[5]  W. Singer,et al.  Deoxyglucose mapping in the cat visual cortex following carotid artery injection and cortical flat-mounting , 1987, Journal of Neuroscience Methods.

[6]  S. Levay,et al.  Ocular dominance columns and their development in layer IV of the cat's visual cortex: A quantitative study , 1978, The Journal of comparative neurology.

[7]  W. Singer,et al.  Changes in the circuitry of the kitten visual cortex are gated by postsynaptic activity , 1979, Nature.

[8]  D. Hubel,et al.  Anatomical demonstration of orientation columns in macaque monkey , 1978, The Journal of comparative neurology.

[9]  D. Hubel,et al.  Projection into the visual field of ocular dominance columns in macaque monkey , 1977, Brain Research.

[10]  G. Blasdel,et al.  Voltage-sensitive dyes reveal a modular organization in monkey striate cortex , 1986, Nature.

[11]  W. Singer,et al.  Topographic organization of the orientation column system in large flat‐mounts of the cat visual cortex: A 2‐deoxyglucose study , 1987, The Journal of comparative neurology.

[12]  C. Malsburg,et al.  Outline of a theory for the ontogenesis of iso-orientation domains in visual cortex , 1982, Biological Cybernetics.

[13]  David H. Hubel,et al.  An autoradiographic study of the retino-cortical projections in the tree shrew (Tupaia glis) , 1975, Brain Research.

[14]  K. Albus,et al.  14C-Deoxyglucose mapping of orientation subunits in the cats visual cortical areas , 2004, Experimental Brain Research.

[15]  D. Hubel,et al.  Plasticity of ocular dominance columns in monkey striate cortex. , 1977, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[16]  D. Hubel,et al.  Anatomical Demonstration of Columns in the Monkey Striate Cortex , 1969, Nature.

[17]  D. Hubel,et al.  Sequence regularity and geometry of orientation columns in the monkey striate cortex , 1974, The Journal of comparative neurology.

[18]  D. Hubel,et al.  Shape and arrangement of columns in cat's striate cortex , 1963, The Journal of physiology.

[19]  W. Singer Topographic organization of orientation columns in the cat visual cortex , 1981, Experimental Brain Research.

[20]  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.

[21]  A L Humphrey,et al.  Topographic organization of the orientation column system in the striate cortex of the tree shrew (Tupaia glis). II. Deoxyglucose mapping , 1980, The Journal of comparative neurology.

[22]  N. Swindale A model for the formation of ocular dominance stripes , 1980, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[23]  W. C. Hall,et al.  Deoxyglucose mapping of the orientation column system in the striate cortex of the tree shrew, Tupaia glis , 1978, Brain Research.

[24]  D. Mitchell,et al.  Monocular astigmatism effects on kitten visual cortex development , 1977, Nature.

[25]  D. Hubel,et al.  Laminar and columnar distribution of geniculo‐cortical fibers in the macaque monkey , 1972, The Journal of comparative neurology.

[26]  W. Singer,et al.  Restriction of visual experience to a single orientation affects the organization of orientation columns in cat visual cortex , 1981, Experimental Brain Research.

[27]  T. Wiesel,et al.  The distribution of afferents representing the right and left eyes in the cat's visual cortex , 1977, Brain Research.

[28]  V. Mountcastle Modality and topographic properties of single neurons of cat's somatic sensory cortex. , 1957, Journal of neurophysiology.

[29]  E. Switkes,et al.  Deoxyglucose analysis of retinotopic organization in primate striate cortex. , 1982, Science.

[30]  D H Hubel,et al.  Autoradiographic demonstration of ocular-dominance columns in the monkey striate cortex by means of transneuronal transport. , 1974, Brain research.

[31]  D. Hubel,et al.  Orientation columns in macaque monkey visual cortex demonstrated by the 2-deoxyglucose autoradiographic technique , 1977, Nature.

[32]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[33]  W. Singer,et al.  The pattern of ocular dominance columns in flat-mounts of the cat visual cortex , 2004, Experimental Brain Research.

[34]  A. L. Humphrey,et al.  Background and stimulus-induced patterns of high metabolic activity in the visual cortex (area 17) of the squirrel and macaque monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  D. Hubel,et al.  Anatomy and physiology of a color system in the primate visual cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  S. Levay,et al.  The complete pattern of ocular dominance stripes in the striate cortex and visual field of the macaque monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  M. Stryker,et al.  Ocular dominance in layer IV of the cat's visual cortex and the effects of monocular deprivation. , 1978, The Journal of physiology.