Tangential intracortical pathways and the development of iso-orientation bands in cat striate cortex.

Evidence is accumulating that tangential connections are a prominent feature of cortical organization. In the mammalian visual cortex, these connections appear to be related to columnar systems and theoretical considerations have suggested that they contribute to the development of regularly spaced orientation columns. We tested this assumption and examined whether early cortical lesions affected the formation and layout of the pattern of iso-orientation bands. In the striate cortex of 2-week-old kittens, tangential fiber paths were disrupted unilaterally along the representation of the horizontal meridian either by cuts, or by suction or by implanting pieces of Teflon. At this age, tangential fibers are still growing, orientation selectivity is only poorly developed and 2-deoxyglucose mapping does not yet reveal orientation columns. When the kittens were 7-10 weeks old, the organization of orientation bands was studied with the 2-deoxyglucose technique in flat-mounts of both visual cortices. In addition, kittens from the same litters as the experimental animals, having received the same lesions at the same postnatal day were subjected to neuroanatomical experiments to assess the effect of the lesion on the tangential fibers. These investigations revealed that a small fraction of tangential fibers had grown across the lesion when no mechanical barrier was implanted while disruption of tangential connections was complete in cases who had received Teflon implants. Apart from minor irregularities that were confined to the vicinity of the lesion, the 2-deoxyglucose experiments showed no differences in the pattern of orientation bands between the lesioned and intact hemispheres. In both, the bands extended throughout all cortical layers and their main trajectories were orthogonal to the representation of the vertical meridian. We conclude that at least from two weeks of age onwards, intracortical tangential connections are not necessary for the development of the regular pattern of iso-orientation bands in the striate cortex of cats.

[1]  M. Imbert,et al.  Visual cortical cells: their developmental properties in normal and dark reared kittens. , 1976, The Journal of physiology.

[2]  J. Pettigrew,et al.  The effect of visual experience on the development of stimulus specificity by kitten cortical neurones , 1974, The Journal of physiology.

[3]  N. Swindale,et al.  A model for the formation of orientation columns , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[4]  G. Mitchison,et al.  Long axons within the striate cortex: their distribution, orientation, and patterns of connection. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[5]  E. Callaway,et al.  Emergence and refinement of clustered horizontal connections in cat striate cortex , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  C. Blakemore,et al.  Innate and environmental factors in the development of the kitten's visual cortex. , 1975, The Journal of physiology.

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

[8]  J. Clarke,et al.  Is there a correlation between continuous neurogenesis and directed axon regeneration in the vertebrate nervous system? , 1988, Trends in Neurosciences.

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

[10]  T. Tsumoto,et al.  Postnatal development of the corticofugal projection from striate cortex to lateral geniculate nucleus in kittens. , 1982, Brain research.

[11]  J. Szentágothai Synaptology of the Visual Cortex , 1973 .

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

[13]  M. Schwab,et al.  Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors , 1990, Nature.

[14]  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.

[15]  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.

[16]  Y. Frégnac,et al.  Early development of visual cortical cells in normal and dark‐reared kittens: relationship between orientation selectivity and ocular dominance. , 1978, The Journal of physiology.

[17]  A. L. Humphrey,et al.  Anatomical banding of intrinsic connections in striate cortex of tree shrews (Tupaia glis) , 1982, The Journal of comparative neurology.

[18]  S. Levay,et al.  Patchy intrinsic projections in visual cortex, area 18, of the cat: Morphological and immunocytochemical evidence for an excitatory function , 1988, The Journal of comparative neurology.

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

[20]  M. Reivich,et al.  THE [14C]DEOXYGLUCOSE METHOD FOR THE MEASUREMENT OF LOCAL CEREBRAL GLUCOSE UTILIZATION: THEORY, PROCEDURE, AND NORMAL VALUES IN THE CONSCIOUS AND ANESTHETIZED ALBINO RAT 1 , 1977, Journal of neurochemistry.

[21]  J. Lund,et al.  Intrinsic laminar lattice connections in primate visual cortex , 1983, The Journal of comparative neurology.

[22]  A. Burkhalter,et al.  Fluorescent latex microspheres as a retrograde neuronal marker for in vivo and in vitro studies of visual cortex , 1984, Nature.

[23]  M. Berry,et al.  Deposition of scar tissue in the central nervous system. , 1983, Acta neurochirurgica. Supplementum.

[24]  D. Hubel,et al.  Receptive fields of single neurones in the cat's striate cortex , 1959, The Journal of physiology.

[25]  Charles D. Gilbert,et al.  The Role of Horizontal Connections in Generating Long Receptive Fields in the Cat Visual Cortex , 1989, The European journal of neuroscience.

[26]  D. Hubel,et al.  RECEPTIVE FIELDS OF CELLS IN STRIATE CORTEX OF VERY YOUNG, VISUALLY INEXPERIENCED KITTENS. , 1963, Journal of neurophysiology.

[27]  M. Cynader,et al.  Intrinsic projections within visual cortex: evidence for orientation-specific local connections. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[28]  M. Cynader,et al.  Anatomical properties and physiological correlates of the intrinsic connections in cat area 18 , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  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.

[30]  K. Albus,et al.  Early post‐natal development of neuronal function in the kitten's visual cortex: a laminar analysis. , 1984, The Journal of physiology.

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

[32]  C. Blakemore,et al.  Development of orientation columns in cat striate cortex revealed by 2-deoxyglucose autoradiography , 1983, Nature.

[33]  J. Lund,et al.  Widespread periodic intrinsic connections in the tree shrew visual cortex. , 1982, Science.

[34]  H. J. Luhmann,et al.  Horizontal Interactions in Cat Striate Cortex: I. Anatomical Substrate and Postnatal Development , 1990, The European journal of neuroscience.

[35]  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.

[36]  T. Wiesel,et al.  Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  D. Whitteridge,et al.  Form, function and intracortical projections of spiny neurones in the striate visual cortex of the cat. , 1984, The Journal of physiology.

[38]  T. Powell,et al.  The intrinsic, association and commissural connections of area 17 on the visual cortex. , 1975, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[39]  L. Palmer,et al.  The retinotopic organization of area 17 (striate cortex) in the cat , 1978, The Journal of comparative neurology.

[40]  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.

[41]  A. B. Bonds Development of Orientation Tuning in the Visual Cortex of Kittens , 1979 .

[42]  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.

[43]  D. Bodian A new method for staining nerve fibers and nerve endings in mounted paraffin sections , 1936 .

[44]  C. Shatz,et al.  The relationship between the geniculocortical afferents and their cortical target cells during development of the cat's primary visual cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  J. Murray How the Leopard Gets Its Spots. , 1988 .