Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1987 Jun;84(11):3936–3940. doi: 10.1073/pnas.84.11.3936

The retinal ganglion cell mosaic defines orientation columns in striate cortex.

R E Soodak
PMCID: PMC304991  PMID: 3108884

Abstract

A computer simulation was used to demonstrate that the tangential organization of orientation columns is a natural consequence of the orderly projection of the mosaic of retinal ganglion cells onto the visual cortex. Parameters of the simulation were taken from published anatomical and electrophysiological data, and the resulting columnar organization of the simulated visual cortex shows many similarities with observations from animals. The model is able to account for a variety of experimental observations, including the presence of orientation columns in visually inexperienced animals.

Full text

PDF
3936

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Albus K. A quantitative study of the projection area of the central and the paracentral visual field in area 17 of the cat. II. The spatial organization of the orientation domain. Exp Brain Res. 1975 Dec 22;24(2):181–202. doi: 10.1007/BF00234062. [DOI] [PubMed] [Google Scholar]
  2. Albus K., Wolf W. Early post-natal development of neuronal function in the kitten's visual cortex: a laminar analysis. J Physiol. 1984 Mar;348:153–185. doi: 10.1113/jphysiol.1984.sp015104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Blakemore C., Cooper G. F. Development of the brain depends on the visual environment. Nature. 1970 Oct 31;228(5270):477–478. doi: 10.1038/228477a0. [DOI] [PubMed] [Google Scholar]
  4. Blakemore C., Van Sluyters R. C. Innate and environmental factors in the development of the kitten's visual cortex. J Physiol. 1975 Jul;248(3):663–716. doi: 10.1113/jphysiol.1975.sp010995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blakemore C., Van Sluyters R. C. Reversal of the physiological effects of monocular deprivation in kittens: further evidence for a sensitive period. J Physiol. 1974 Feb;237(1):195–216. doi: 10.1113/jphysiol.1974.sp010478. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Blasdel G. G., Fitzpatrick D. Physiological organization of layer 4 in macaque striate cortex. J Neurosci. 1984 Mar;4(3):880–895. doi: 10.1523/JNEUROSCI.04-03-00880.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Blasdel G. G., Lund J. S. Termination of afferent axons in macaque striate cortex. J Neurosci. 1983 Jul;3(7):1389–1413. doi: 10.1523/JNEUROSCI.03-07-01389.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Blasdel G. G., Salama G. Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature. 1986 Jun 5;321(6070):579–585. doi: 10.1038/321579a0. [DOI] [PubMed] [Google Scholar]
  9. Boycott B. B., Wässle H. The morphological types of ganglion cells of the domestic cat's retina. J Physiol. 1974 Jul;240(2):397–419. doi: 10.1113/jphysiol.1974.sp010616. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Braitenberg V., Braitenberg C. Geometry of orientation columns in the visual cortex. Biol Cybern. 1979 Aug 1;33(3):179–186. doi: 10.1007/BF00337296. [DOI] [PubMed] [Google Scholar]
  11. Buisseret P., Imbert M. Visual cortical cells: their developmental properties in normal and dark reared kittens. J Physiol. 1976 Feb;255(2):511–525. doi: 10.1113/jphysiol.1976.sp011293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Bullier J., Henry G. H. Neural path taken by afferent streams in striate cortex of the cat. J Neurophysiol. 1979 Sep;42(5):1264–1270. doi: 10.1152/jn.1979.42.5.1264. [DOI] [PubMed] [Google Scholar]
  13. Bullier J., Henry G. H. Ordinal position and afferent input of neurons in monkey striate cortex. J Comp Neurol. 1980 Oct 15;193(4):913–935. doi: 10.1002/cne.901930407. [DOI] [PubMed] [Google Scholar]
  14. Campbell F. W., Cleland B. G., Cooper G. F., Enroth-Cugell C. The angular selectivity of visual cortical cells to moving gratings. J Physiol. 1968 Sep;198(1):237–250. doi: 10.1113/jphysiol.1968.sp008604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Cleland B. G., Dubin M. W., Levick W. R. Sustained and transient neurones in the cat's retina and lateral geniculate nucleus. J Physiol. 1971 Sep;217(2):473–496. doi: 10.1113/jphysiol.1971.sp009581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Cooper L. N., Liberman F., Oja E. A theory for the acquisition and loss of neuron specificity in visual cortex. Biol Cybern. 1979 Jun 29;33(1):9–28. doi: 10.1007/BF00337414. [DOI] [PubMed] [Google Scholar]
  17. De Monasterio F. M., Gouras P. Functional properties of ganglion cells of the rhesus monkey retina. J Physiol. 1975 Sep;251(1):167–195. doi: 10.1113/jphysiol.1975.sp011086. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. De Valois K. K., De Valois R. L., Yund E. W. Responses of striate cortex cells to grating and checkerboard patterns. J Physiol. 1979 Jun;291:483–505. doi: 10.1113/jphysiol.1979.sp012827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Derrington A. M., Fuchs A. F. The development of spatial-frequency selectivity in kitten striate cortex. J Physiol. 1981 Jul;316:1–10. doi: 10.1113/jphysiol.1981.sp013767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Derrington A. M., Lennie P. Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. J Physiol. 1984 Dec;357:219–240. doi: 10.1113/jphysiol.1984.sp015498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Dow B. M., Bauer R. Retinotopy and orientation columns in the monkey: a new model. Biol Cybern. 1984;49(3):189–200. doi: 10.1007/BF00334465. [DOI] [PubMed] [Google Scholar]
  22. Enroth-Cugell C., Robson J. G. The contrast sensitivity of retinal ganglion cells of the cat. J Physiol. 1966 Dec;187(3):517–552. doi: 10.1113/jphysiol.1966.sp008107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ferster D., LeVay S. The axonal arborizations of lateral geniculate neurons in the striate cortex of the cat. J Comp Neurol. 1978 Dec 15;182(4 Pt 2):923–944. doi: 10.1002/cne.901820510. [DOI] [PubMed] [Google Scholar]
  24. Fitzpatrick D., Itoh K., Diamond I. T. The laminar organization of the lateral geniculate body and the striate cortex in the squirrel monkey (Saimiri sciureus). J Neurosci. 1983 Apr;3(4):673–702. doi: 10.1523/JNEUROSCI.03-04-00673.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Freund T. F., Martin K. A., Whitteridge D. Innervation of cat visual areas 17 and 18 by physiologically identified X- and Y- type thalamic afferents. I. Arborization patterns and quantitative distribution of postsynaptic elements. J Comp Neurol. 1985 Dec 8;242(2):263–274. doi: 10.1002/cne.902420208. [DOI] [PubMed] [Google Scholar]
  26. Gouras P. Antidromic responses of orthodromically identified ganglion cells in monkey retina. J Physiol. 1969 Oct;204(2):407–419. doi: 10.1113/jphysiol.1969.sp008920. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. HUBEL D. H., WIESEL T. N. Integrative action in the cat's lateral geniculate body. J Physiol. 1961 Feb;155:385–398. doi: 10.1113/jphysiol.1961.sp006635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. HUBEL D. H., WIESEL T. N. RECEPTIVE FIELDS OF CELLS IN STRIATE CORTEX OF VERY YOUNG, VISUALLY INEXPERIENCED KITTENS. J Neurophysiol. 1963 Nov;26:994–1002. doi: 10.1152/jn.1963.26.6.994. [DOI] [PubMed] [Google Scholar]
  29. HUBEL D. H., WIESEL T. N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol. 1962 Jan;160:106–154. doi: 10.1113/jphysiol.1962.sp006837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. HUBEL D. H., WIESEL T. N. Shape and arrangement of columns in cat's striate cortex. J Physiol. 1963 Mar;165:559–568. doi: 10.1113/jphysiol.1963.sp007079. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Hammond P. Cat retinal ganglion cells: size and shape of receptive field centres. J Physiol. 1974 Oct;242(1):99–118. doi: 10.1113/jphysiol.1974.sp010696. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Hendrickson A. E., Wilson J. R., Ogren M. P. The neuroanatomical organization of pathways between the dorsal lateral geniculate nucleus and visual cortex in Old World and New World primates. J Comp Neurol. 1978 Nov 1;182(1):123–136. doi: 10.1002/cne.901820108. [DOI] [PubMed] [Google Scholar]
  33. Hirsch H. V., Spinelli D. N. Visual experience modifies distribution of horizontally and vertically oriented receptive fields in cats. Science. 1970 May 15;168(3933):869–871. doi: 10.1126/science.168.3933.869. [DOI] [PubMed] [Google Scholar]
  34. Hochstein S., Shapley R. M. Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. J Physiol. 1976 Nov;262(2):265–284. doi: 10.1113/jphysiol.1976.sp011595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Hochstein S., Shapley R. M. Quantitative analysis of retinal ganglion cell classifications. J Physiol. 1976 Nov;262(2):237–264. doi: 10.1113/jphysiol.1976.sp011594. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Horton J. C., Hubel D. H. Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey. Nature. 1981 Aug 20;292(5825):762–764. doi: 10.1038/292762a0. [DOI] [PubMed] [Google Scholar]
  37. Hubel D. H., Wiesel T. N. Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey. J Comp Neurol. 1972 Dec;146(4):421–450. doi: 10.1002/cne.901460402. [DOI] [PubMed] [Google Scholar]
  38. Hubel D. H., Wiesel T. N. Sequence regularity and geometry of orientation columns in the monkey striate cortex. J Comp Neurol. 1974 Dec 1;158(3):267–293. doi: 10.1002/cne.901580304. [DOI] [PubMed] [Google Scholar]
  39. Humphrey A. L., Hendrickson A. E. Background and stimulus-induced patterns of high metabolic activity in the visual cortex (area 17) of the squirrel and macaque monkey. J Neurosci. 1983 Feb;3(2):345–358. doi: 10.1523/JNEUROSCI.03-02-00345.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Humphrey A. L., Sur M., Uhlrich D. J., Sherman S. M. Projection patterns of individual X- and Y-cell axons from the lateral geniculate nucleus to cortical area 17 in the cat. J Comp Neurol. 1985 Mar 8;233(2):159–189. doi: 10.1002/cne.902330203. [DOI] [PubMed] [Google Scholar]
  41. Imbert M., Buisseret P. Receptive field characteristics and plastic properties of visual cortical cells in kittens reared with or without visual experience. Exp Brain Res. 1975;22(1):25–36. doi: 10.1007/BF00235409. [DOI] [PubMed] [Google Scholar]
  42. Kaplan E., Marcus S., So Y. T. Effects of dark adaptation on spatial and temporal properties of receptive fields in cat lateral geniculate nucleus. J Physiol. 1979 Sep;294:561–580. doi: 10.1113/jphysiol.1979.sp012946. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Kaplan E., Shapley R. M. The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. Proc Natl Acad Sci U S A. 1986 Apr;83(8):2755–2757. doi: 10.1073/pnas.83.8.2755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Kaplan E., Shapley R. M. X and Y cells in the lateral geniculate nucleus of macaque monkeys. J Physiol. 1982 Sep;330:125–143. doi: 10.1113/jphysiol.1982.sp014333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Kaplan E., Shapley R. The origin of the S (slow) potential in the mammalian lateral geniculate nucleus. Exp Brain Res. 1984;55(1):111–116. doi: 10.1007/BF00240504. [DOI] [PubMed] [Google Scholar]
  46. Kennedy H., Bullier J., Dehay C. Cytochrome oxidase activity in the striate cortex and lateral geniculate nucleus of the newborn and adult macaque monkey. Exp Brain Res. 1985;61(1):204–209. doi: 10.1007/BF00235636. [DOI] [PubMed] [Google Scholar]
  47. Leventhal A. G., Hirsch H. V. Receptive-field properties of different classes of neurons in visual cortex of normal and dark-reared cats. J Neurophysiol. 1980 Apr;43(4):1111–1132. doi: 10.1152/jn.1980.43.4.1111. [DOI] [PubMed] [Google Scholar]
  48. Leventhal A. G. Relationship between preferred orientation and receptive field position of neurons in cat striate cortex. J Comp Neurol. 1983 Nov 10;220(4):476–483. doi: 10.1002/cne.902200409. [DOI] [PubMed] [Google Scholar]
  49. Levick W. R., Thibos L. N. Analysis of orientation bias in cat retina. J Physiol. 1982 Aug;329:243–261. doi: 10.1113/jphysiol.1982.sp014301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Levick W. R., Thibos L. N. Orientation bias of cat retinal ganglion cells. Nature. 1980 Jul 24;286(5771):389–390. doi: 10.1038/286389a0. [DOI] [PubMed] [Google Scholar]
  51. Linsker R. From basic network principles to neural architecture: emergence of orientation-selective cells. Proc Natl Acad Sci U S A. 1986 Nov;83(21):8390–8394. doi: 10.1073/pnas.83.21.8390. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Livingstone M. S., Hubel D. H. Anatomy and physiology of a color system in the primate visual cortex. J Neurosci. 1984 Jan;4(1):309–356. doi: 10.1523/JNEUROSCI.04-01-00309.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Livingstone M. S., Hubel D. H. Thalamic inputs to cytochrome oxidase-rich regions in monkey visual cortex. Proc Natl Acad Sci U S A. 1982 Oct;79(19):6098–6101. doi: 10.1073/pnas.79.19.6098. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Movshon J. A. Reversal of the physiological effects of monocular deprivation in the kitten's visual cortex. J Physiol. 1976 Sep;261(1):125–174. doi: 10.1113/jphysiol.1976.sp011551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Nass M. M., Cooper L. N. A theory for the development of feature detecting cells in visual cortex. Biol Cybern. 1975 Aug 1;19(1):1–18. doi: 10.1007/BF00319777. [DOI] [PubMed] [Google Scholar]
  56. Perry V. H., Cowey A. The ganglion cell and cone distributions in the monkey's retina: implications for central magnification factors. Vision Res. 1985;25(12):1795–1810. doi: 10.1016/0042-6989(85)90004-5. [DOI] [PubMed] [Google Scholar]
  57. Perry V. H., Oehler R., Cowey A. Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience. 1984 Aug;12(4):1101–1123. doi: 10.1016/0306-4522(84)90006-x. [DOI] [PubMed] [Google Scholar]
  58. Pettigrew J. D. The effect of visual experience on the development of stimulus specificity by kitten cortical neurones. J Physiol. 1974 Feb;237(1):49–74. doi: 10.1113/jphysiol.1974.sp010469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Rauschecker J. P., Singer W. The effects of early visual experience on the cat's visual cortex and their possible explanation by Hebb synapses. J Physiol. 1981 Jan;310:215–239. doi: 10.1113/jphysiol.1981.sp013545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Schall J. D., Vitek D. J., Leventhal A. G. Retinal constraints on orientation specificity in cat visual cortex. J Neurosci. 1986 Mar;6(3):823–836. doi: 10.1523/JNEUROSCI.06-03-00823.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Shapley R., Kaplan E., Soodak R. Spatial summation and contrast sensitivity of X and Y cells in the lateral geniculate nucleus of the macaque. Nature. 1981 Aug 6;292(5823):543–545. doi: 10.1038/292543a0. [DOI] [PubMed] [Google Scholar]
  62. Sherk H., Stryker M. P. Quantitative study of cortical orientation selectivity in visually inexperienced kitten. J Neurophysiol. 1976 Jan;39(1):63–70. doi: 10.1152/jn.1976.39.1.63. [DOI] [PubMed] [Google Scholar]
  63. Singer W. Central control of developmental plasticity in the mammalian visual cortex. Vision Res. 1985;25(3):389–396. doi: 10.1016/0042-6989(85)90064-1. [DOI] [PubMed] [Google Scholar]
  64. So Y. T., Shapley R. Spatial tuning of cells in and around lateral geniculate nucleus of the cat: X and Y relay cells and perigeniculate interneurons. J Neurophysiol. 1981 Jan;45(1):107–120. doi: 10.1152/jn.1981.45.1.107. [DOI] [PubMed] [Google Scholar]
  65. Soodak R. E. Two-dimensional modeling of visual receptive fields using Gaussian subunits. Proc Natl Acad Sci U S A. 1986 Dec;83(23):9259–9263. doi: 10.1073/pnas.83.23.9259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Stone J., Dreher B. Projection of X- and Y-cells of the cat's lateral geniculate nucleus to areas 17 and 18 of visual cortex. J Neurophysiol. 1973 May;36(3):551–567. doi: 10.1152/jn.1973.36.3.551. [DOI] [PubMed] [Google Scholar]
  67. Stryker M. P., Sherk H., Leventhal A. G., Hirsch H. V. Physiological consequences for the cat's visual cortex of effectively restricting early visual experience with oriented contours. J Neurophysiol. 1978 Jul;41(4):896–909. doi: 10.1152/jn.1978.41.4.896. [DOI] [PubMed] [Google Scholar]
  68. Swindale N. V. A model for the formation of orientation columns. Proc R Soc Lond B Biol Sci. 1982 May 22;215(1199):211–230. doi: 10.1098/rspb.1982.0038. [DOI] [PubMed] [Google Scholar]
  69. Tanaka K. Cross-correlation analysis of geniculostriate neuronal relationships in cats. J Neurophysiol. 1983 Jun;49(6):1303–1318. doi: 10.1152/jn.1983.49.6.1303. [DOI] [PubMed] [Google Scholar]
  70. Tootell R. B., Silverman M. S., Switkes E., De Valois R. L. Deoxyglucose analysis of retinotopic organization in primate striate cortex. Science. 1982 Nov 26;218(4575):902–904. doi: 10.1126/science.7134981. [DOI] [PubMed] [Google Scholar]
  71. Tusa R. J., Palmer L. A., Rosenquist A. C. The retinotopic organization of area 17 (striate cortex) in the cat. J Comp Neurol. 1978 Jan 15;177(2):213–235. doi: 10.1002/cne.901770204. [DOI] [PubMed] [Google Scholar]
  72. Van Essen D. C., Newsome W. T., Maunsell J. H. The visual field representation in striate cortex of the macaque monkey: asymmetries, anisotropies, and individual variability. Vision Res. 1984;24(5):429–448. doi: 10.1016/0042-6989(84)90041-5. [DOI] [PubMed] [Google Scholar]
  73. Weber J. T., Huerta M. F., Kaas J. H., Harting J. K. The projections of the lateral geniculate nucleus of the squirrel monkey: studies of the interlaminar zones and the S layers. J Comp Neurol. 1983 Jan 10;213(2):135–145. doi: 10.1002/cne.902130203. [DOI] [PubMed] [Google Scholar]
  74. Wiesel T. N., Hubel D. H. Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. J Neurophysiol. 1966 Nov;29(6):1115–1156. doi: 10.1152/jn.1966.29.6.1115. [DOI] [PubMed] [Google Scholar]
  75. Wässle H., Boycott B. B., Illing R. B. Morphology and mosaic of on- and off-beta cells in the cat retina and some functional considerations. Proc R Soc Lond B Biol Sci. 1981 May 22;212(1187):177–195. doi: 10.1098/rspb.1981.0033. [DOI] [PubMed] [Google Scholar]
  76. Wässle H., Levick W. R., Cleland B. G. The distribution of the alpha type of ganglion cells in the cat's retina. J Comp Neurol. 1975 Feb 1;159(3):419–438. doi: 10.1002/cne.901590308. [DOI] [PubMed] [Google Scholar]
  77. Wässle H., Peichl L., Boycott B. B. Morphology and topography of on- and off-alpha cells in the cat retina. Proc R Soc Lond B Biol Sci. 1981 May 22;212(1187):157–175. doi: 10.1098/rspb.1981.0032. [DOI] [PubMed] [Google Scholar]
  78. von der Malsburg C., Cowan J. D. Outline of a theory for the ontogenesis of iso-orientation domains in visual cortex. Biol Cybern. 1982;45(1):49–56. doi: 10.1007/BF00387213. [DOI] [PubMed] [Google Scholar]
  79. von der Malsburg C. Self-organization of orientation sensitive cells in the striate cortex. Kybernetik. 1973 Dec 31;14(2):85–100. doi: 10.1007/BF00288907. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES