Experimental Brain Research

, Volume 41, Issue 3–4, pp 199–215

Restriction of visual experience to a single orientation affects the organization of orientation columns in cat visual cortex

A study with deoxyglucose
  • W. Singer
  • B. Freeman
  • J. Rauschecker

Summary and Conclusions

In six dark reared, 4-weak-old kittens visual experience was restricted to contours of a single orientation, horizontal or vertical, using cylindrical lenses. Subsequently, the deoxyglucose method was used to determine whether these artificial raising conditions had affected the development of orientation columns in the visual cortex. After application of the deoxyglucose pulse one hemifield was stimulated with vertical, the other with horizontal contours. Thus, from interhemispheric comparison, changes in columnar systems corresponding to experienced and inexperienced orientations could be determined. The following results were obtained: (1) Irrespective of the restrictions in visual experience, orientation columns develop in areas 17, 18, 19 and in the visual areas of the posterior suprasylvian sulcus. (2) Within area 17, spacing between columns encoding the same orientations is remarkably regular (1 mm), is not influenced by selective experience and shows only slight interindividual variation. (3) In non-striate areas the spacing of columns is less regular and the spatial frequency of the periodicity is lower. (4) The modifiability of this columnar pattern by selective experience is small within the granular layer of striate cortex but substantial in non-granular layers: Within layer IV columns whose preference corresponds to the experienced orientation are wider and more active than those encoding the orthogonal orientation but the columnar grid remains basically unaltered. Outside layer IV the columnar system is maintained only for columns encoding the experienced orientations. The deprived columns by contrast frequently fail to extend into non-granular layers and remain confined to the vicinity of layer IV. (5) These modifications in the columnar arrangement are more pronounced in striate cortex than in non-striate visual areas and, within the former, more conspicuous in the central than in the peripheral representation of the visual field. It is concluded that within layer IV the blue print for the system of orientation columns is determined by genetic instructions: first order cells in layer IV develop orientation selectivity irrespective of experience whereby the preference for a particular orientation is predetermined by the position in the columnar grid. Dependent on experience is, however, the expansion of the columnar system from layer IV into non-granular layers. It is argued that all distortions following selective rearing can be accounted for by competitive interactions between intracortical pathways, the mechanisms being identical to those established for competitive processes in the domain of ocular dominance columns. It is proposed that such experience dependent modifiability of connections between first and second order cells is a necessary prerequisite for the development of orientation selectivity in cells with large and complex receptive fields.

Key words

Visual cortex Development Orientation columns Deoxyglucose 


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  1. Albus K (1975a) A quantitative study of the projection area of the central and the paracentral visual field in area 17 of the cat. I. The precision of the topography. Exp Brain Res 24: 159–179Google Scholar
  2. Albus K (1975b) 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 24: 181–202Google Scholar
  3. Albus K (1979) 14C-deoxyglucose mapping of orientation subum'ts in the cats visual cortical areas. Exp Brain Res 37: 609–613Google Scholar
  4. Barlow HB (1975) Visual experience and cortical development. Nature 258: 199–204Google Scholar
  5. Blakemore C, Cooper GF (1970) Development of the brain depends on the visual environment. Nature 228: 477–478Google Scholar
  6. Blakemore C, Van Sluyters RC (1975) Innate and environmental factors in the development of the kitten's visual cortex. J Physiol (Lond) 248: 663–716Google Scholar
  7. Blasdel GG, Mitchell DE, Muir DW, Pettigrew JD (1977) A physiological and behavioural study in cats of the effect of early visual experience with contours of a single orientation. J Physiol (Lond) 265: 615–636Google Scholar
  8. Buisseret P, Imbert M (1976) Visual cortical cells. Their developmental properties in normal and dark reared kittens. J Physiol (Lond) 255: 511–525Google Scholar
  9. Creutzfeldt OD, Innocenti GM, Brooks D (1974) Vertical organization in the visual cortex (Area 17). Exp Brain Res 21: 315–336Google Scholar
  10. Creutzfeldt OD, Garey LJ, Kuroda R, Wolff JR (1977) The distribution of degenerating axons after small lesions in the intact and isolated visual cortex of the cat. Exp Brain Res 27: 419–440Google Scholar
  11. Cynader M, Mitchell DE (1977) Monocular astigmatism effects on kitten visual cortex development. Nature 270: 177–178Google Scholar
  12. Fisken RA, Garey LJ, Powell TPS (1973) Patterns of degeneration after intrinsic lesions of the visual cortex (Area 17) of the monkey. Brain Res 53: 208–213Google Scholar
  13. Flood DG, Coleman PD (1979) Demonstration of orientation columns with [C14]-2-deoxyglucose in a cat reared in a striped environment. Brain Res 173: 538–542Google Scholar
  14. Freeman RD, Pettigrew JD (1973) Alteration of visual cortex from environmental asymmetries. Nature 246: 359–360Google Scholar
  15. Freeman RD, Thibos LN (1975a) Contrast sensitivity in humans with abnormal visual experience. J Physiol (Lond) 247: 687–710Google Scholar
  16. Freeman RD, Thibos LN (1975b) Visual evoked responses in humans with abnormal visual experience. J Physiol (Lond) 247: 711–724Google Scholar
  17. Fregnac Y, Imbert M (1978) Early development of visual cortical cells in normal and dark-reared kittens. Relationship between orientation selectivity and ocular dominance. J Physiol (Lond) 278: 27–44Google Scholar
  18. Hebb DO (1949) The organization of behaviour. Wiley, New YorkGoogle Scholar
  19. Henry GH, Dreher B, Bishop PO (1974) Orientation specificity of cells in cat striate cortex. J Neurophysiol 37: 1394–1409Google Scholar
  20. Hirsch HVB, Spinelli DN (1970) Visual experience modifies distribution of horizontally and vertically oriented receptive fields in cats. Science 168: 869–871Google Scholar
  21. Hirsch HVB, Spinelli DN (1971) Modification of the distribution of receptive field orientation in cats by selective visual exposure during development. Exp Brain Res 13: 509–527Google Scholar
  22. Hubel DH, Wiesel TN (1962) Receptive fields, binocular interaction, and functional architecture in the cat's visual cortex. J Physiol (Lond) 160: 106–154Google Scholar
  23. Hubel DH, Wiesel TN (1963a) Shape and arrangement of columns in cat's striate cortex. J Physiol (Lond) 160: 106–154Google Scholar
  24. Hubel DH, Wiesel TN (1963b) Receptive fields of cells in striate cortex of very young, visually inexperienced kittens. J Neurophysiol 26: 994–1002PubMedGoogle Scholar
  25. Hubel DH, Wiesel TN (1965) Receptive fields and functional architecture in two non-striate visual areas (18 and 19) of the cat. J Neurophysiol 28: 229–289Google Scholar
  26. Hubel DH, Wiesel TN (1974a) Sequence regularity and geometry of orientation columns in the monkey striate cortex. J Comp Neurol 158: 267–294Google Scholar
  27. Hubel DH, Wiesel TN (1974b) Uniformity of monkey striate cortex. A parallel relationship between field size, scatter and magnification factor. J Comp Neurol 158: 295–306Google Scholar
  28. Hubel DH, Wiesel TN, LeVay S (1977a) Plasticity of ocular dominance columns in monkey striate cortex. Phil Trans R Soc Lond [Biol] 278: 377–409Google Scholar
  29. Hubel DH, Wiesel TN, Stryker MP (1977b) Orientation columns in macaque monkey demonstrated by the 2-deoxyglucose autoradiographic technique. Nature 269: 328–330Google Scholar
  30. Hubel DH, Wiesel TN, Stryker MP (1978) Anatomical demonstration of orientation columns in macaque monkey. J Comp Neurol 177: 361–380Google Scholar
  31. Imbert M, Buisseret P (1975) Receptive field characteristics and plastic properties of visual cortical cells in kittens reared with or without visual experience. Exp Brain Res 22: 25–36Google Scholar
  32. Lund JS, Henry GH, MacQueen CL, Harvey AR (1979) Anatomical organization of the primary visual cortex (Area 17) of the cat. A comparison with Area 17 of the macaque monkey. J Comp Neurol 184: 599–618Google Scholar
  33. Mitchell DE, Wilkinson F (1974) The effect of early astigmatism on the visual resolution of gratings. J Physiol (Lond) 243: 739–756Google Scholar
  34. Mitchell DE, Freeman RD, Millodot M, Haegerstrom G (1973) Meridional amblyopia: evidence for modification of the human visual system by early visual experience. Vision Res 13: 535–558Google Scholar
  35. Mitzdorf U, Singer W (1978) Prominent excitatory pathways in the cat visual cortex (A17 and A18). A current source density analysis of electrically evoked potentials. Exp Brain Res 33: 371–394Google Scholar
  36. Palmer LA, Rosenquist AC, Tusa RJ (1978) The retinotopic organization of lateral suprasylvian visual areas in the cat. J Comp Neurol 177: 237–256Google Scholar
  37. Pettigrew JD (1978) The paradox of the critical period for striate cortex.In: Cotman CW (ed) Neuronal plasticity. Raven Press, New York, pp 311–330Google Scholar
  38. Pettigrew JD, Olson C, Hirsch HVB (1973) Cortical effect of selective visual experience. Degeneration or reorganization? Brain Res 51: 345–351Google Scholar
  39. Rauschecker JP (1979) Orientation-dependent changes in response properties of neurons in the kitten's visual cortex. In: Freeman RD (ed) Developmental neurobiology of vision. Plenum Press, New York, pp 121–133Google Scholar
  40. Rauschecker JP, Singer W (1979) Changes in the circuitry of the kitten's visual cortex are gated by postsynaptic activity. Nature 280: 58–60Google Scholar
  41. Rauschecker JP, Singer W (1981) The effects of early visual experience on the cat's visual cortex and their possible explanation by Hebb synapses. J Physiol (Lond) 310Google Scholar
  42. Shatz CJ, Lindstrom S, Wiesel TN (1977) The distribution of afferents representing the right and left eyes in the cats visual cortex. Brain Res 131: 103–116Google Scholar
  43. Sherk H, Stryker MP (1976) Quantitative study of cortical orientation selectivity in visually inexperienced kittens. J Neurophysiol 39: 63–70Google Scholar
  44. Singer W (1976) Modification of orientation and direction selectivity of cortical cells in kittens with monocular vision. Brain Res 118: 460–468Google Scholar
  45. Singer W, Tretter F (1976) Receptive-field properties and neuronal connectivity in striate and parastriate cortex of contour-deprived cats. J Neurophysiol 39: 613–630Google Scholar
  46. Singer W, Tretter F, Cynader M (1975) Organization of cat striate cortex. A correlation of receptive field properties with afferent and efferent connections. J Neurophysiol 38: 1080–1098Google Scholar
  47. Singer W, von Griinau MW, Rauschecker J (1980) Functional amblyopia in kittens with unilateral exotropia. I. Electrophysiological assessment. Exp Brain Res 40: 294–304Google Scholar
  48. Skeen LC, Humphrey AL, Norton TT, Hall WC (1978) Deoxyglucose mapping of the orientation columns system in the striate cortex of the tree shrew, Tupaia glis. Brain Res 142: 538–545Google Scholar
  49. Sokoloff L, Reivich M, Kennedy C, Des Rosiers MH, Patlak CS, Pettigrew KD, Sakurada O, Shinohara M (1977) The 14C-Deoxyglucose method for the measurement of local cerebral glucose utilization: Theory, procedure, and normal values in the conscious and anesthetized albino rat. J Neurochem 28: 897–916PubMedGoogle Scholar
  50. Stryker MP, Sherk H, Leventhal AG, Hirsch HVB (1978) Physiological consequences for the cat's visual cortex of effectively restricting early visual experience with oriented contours. J Neurophysiol 41: 896–909Google Scholar
  51. Szentágothai J (1973) Synaptology of the visual cortex. In: Jung R (ed) Handbook of sensory physiology, vol VII, 3 B. Springer, Berlin Heidelberg New YorkGoogle Scholar
  52. Szentágothai J (1975) The module concept in cerebral cortex architecture. Brain Res 95: 475–496CrossRefPubMedGoogle Scholar
  53. Toyama K, Matsunami K, Ohno T, Tokashiki S (1974) An intracellular study of neuronal organization in the visual cortex. Brain Res 21: 45–66Google Scholar
  54. Tretter F, Cynader M, Singer W (1975a) Modification of direction selectivity of neurons in the visual cortex of kittens. Brain Res 84: 143–149Google Scholar
  55. Tretter F, Cynader M, Singer W (1975b) Cat parastriate cortex. A primary or secondary visual area? J Neurophysiol 38: 1098–1113Google Scholar
  56. Tusa RT, Rosenquist AC, Palmer LA (1979) Retinotopic organization of areas 18 and 19 in the cat. J Comp Neurol 185: 657–678Google Scholar
  57. Watkins DW, Wilson JR, Sherman SM (1978) Receptive-field properties of neurons in binocular and monocular segments of striate cortex in cats raised with binocular lid suture. J Neurophysiol 41: 322–337Google Scholar
  58. Wiesel TN, Hubel DH (1974) Ordered arrangement of orientation columns in monkeys lacking visual experience. J Comp Neurol 158: 307–318Google Scholar

Copyright information

© Springer-Verlag 1981

Authors and Affiliations

  • W. Singer
    • 1
  • B. Freeman
    • 1
  • J. Rauschecker
    • 1
  1. 1.Max-Planck-Institute for PsychiatryMunich 40Federal Republic of Germany

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