Experimental Brain Research

, Volume 75, Issue 1, pp 117–132 | Cite as

Changing patterns of binocular visual connections in the intertectal system during development of the frog, Xenopus laevis

II. Abnormalities following early visual deprivation
  • S. Grant
  • M. J. Keating


During normal metamorphic and postmetamorphic growth of the frog, Xenopus laevis, there is a major and orderly remodelling of the pattern of neuronal connections in the intertectal system. These changes preserve the spatial registration of binocular visual inputs to each optic tectum in the face of continuous changes in relative eye alignment (Grant and Keating 1989). We suggested that visual experience might be utilised by the intertectal system to effect the maturational remodelling of its connections, with particular involvement in maintaining binocular visual registration. To investigate this suggestion we studied the development of the intertectal system in animals that had been reared in total darkness from before the onset of function in the system. Visual deprivation did not affect the developmental ocular migration that normally occurs in Xenopus, nor did it affect the maturation of the contralateral visuotectal projection. Abnormalities were, however, observed in the ipsilateral visuotectal projection of all dark-reared animals studied, reflecting perturbation of the underlying intertectal system. The abnormalities included disorder and deficits in the projection, which became more marked with age. Quantitative analyses of the spatial registration of binocular visual inputs to the optic tectum revealed that, in all dark-reared animals studied, registration was both significantly poorer and systematically shifted compared to normal controls. Analysis of maturational changes in the pattern of intertectal connections in visually-deprived animals led to the conclusion that intrinsic developmental processes generate an initially well-organised intertectal system and programme much of its continuous expansion with age. Visual experience, however, is necessary for the large scale and orderly remodelling of the system which, during normal maturation, preserves binocular visual registration despite changes in interocular alignment.

Key words

Amphibia Xenopus laevis Binocular visual field Optic tectum Development Intertectal connections Plasticity Dark-rearing 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Berman NE, Murphy EH (1982) The critical period for alteration in cortical binocularity resulting from divergent and convergent strabismus. Dev Brain Res 2: 181–202Google Scholar
  2. Berman NE, Payne BR (1983) Alterations in connections of the corpus callosum following convergent and divergent strabismus. Brain Res 274: 201–212Google Scholar
  3. Blakemore C (1978) Maturation and modification in the developing visual system. In: Held R, Liebowitz HW, Teuber HL (eds) Handbook of sensory physiology, vol VIII. Springer, Berlin Heidelberg New York, pp 377–436Google Scholar
  4. Blakemore C, Van Sluyters RC (1975) Innate and environmental factors in the development of the kittens visual cortex. J Physiol (Lond) 248: 663–716Google Scholar
  5. Dursteler MR, Heydt R von der (1983) Plasticity in the binocular correspondence of striate cortical receptive fields in kittens. J Physiol (Lond) 345: 87–105Google Scholar
  6. Feldman JD, Keating MJ (1983) Intertectal neuronal plasticity in Xenopus laevis: examination of the developmental critical period during which such plasticity is possible. J Physiol (Lond) 336: 29PGoogle Scholar
  7. Gaze RM, Keating MJ, Szekely G, Beazley L (1970) Binocular interaction in the formation of specific intertectal neuronal connexions. Proc R Soc Lond [Biol] 175: 107–147Google Scholar
  8. Grant S (1982) The development and modification of binocular neuronal connections in Xenopus laevis. PhD Thesis, CNNA, LondonGoogle Scholar
  9. Grant S, Keating MJ (1986) Normal maturation involves systematic changes in binocular visual connections in Xenopus laevis. Nature 322: 258–261Google Scholar
  10. Grant S, Keating MJ (1989) Changing patterns of binocular visual connections in the intertectal system during development of the frog, Xenopus laevis. I. Normal maturational changes in response to changing binocular geometry. Exp Brain Res 75: 99–116Google Scholar
  11. Grunau MW von (1979) The role of maturation and visual experience in the development of eye alignment in cats. Exp Brain Res 37: 41–47Google Scholar
  12. Hubel D, Wiesel TN (1965) Binocular interaction in striate cortex of kittens reared with artificial squint. J Neurophysiol 28: 1041–1059Google Scholar
  13. Innocenti GM (1981) Growth and reshaping of axons in the establishment of visual callosal connections. Science 212: 824–827Google Scholar
  14. Innocenti GM, Caminiti R (1980) Postnatal shaping of callosal connections from sensory areas. Exp Brain Res 38: 381–394Google Scholar
  15. Innocenti GM, Frost DO (1979) The effects of visual experience on the maturation of the efferent system in the corpus callosum. Nature 280: 231–234Google Scholar
  16. Innocenti GM, Frost DO (1980) The postnatal development of visual callosal connections in the absence of visual experience or of the eyes. Exp Brain Res 39: 365–375Google Scholar
  17. Keating MJ (1974) The role of visual function in the patterning of binocular visual connections. Br Med Bull 30: 145–151Google Scholar
  18. Keating MJ, Beazley LD, Feldman JD, Gaze RM (1975) Binocular interaction and intertectal neuronal connections in Xenopus laevis — dependence upon developmental stage. Proc R Soc Lond [Biol] 191: 445–466Google Scholar
  19. Keating MJ, Grant S, Dawes EA, Nanchahal K (1986) Visual deprivation and the maturation of the retinotectal projection in Xenopus laevis. J Embryol Exp Morphol 91: 101–115Google Scholar
  20. Keating MJ, Kennard C (1987) Visual experience and the maturation of the ipsilateral visuotectal projection in Xenopus laevis. Neuroscience 21: 519–527Google Scholar
  21. Knudsen EI, Knudsen PF, Esterly SD (1982) Early auditory experience modifies sound localisation in barn owls. Nature 295: 238–240Google Scholar
  22. LeVay S, Stryker MP, Shatz CJ (1978) Ocular domiance columns and their development in layer IV of the cat's visual cortex: a quantitative study. J Comp Neurol 179: 223–244Google Scholar
  23. Levitt FB, Van Sluyters RC (1982) The sensitive period for strabismus in the kitten. Dev Brain Res 3: 323–327Google Scholar
  24. Lund RD, Mitchell DE (1979) The effects of dark-rearing on visual callosal connections of cats. Brain Res 167: 172–175Google Scholar
  25. Lund RD, Mitchell DE, Henry GH (1978) Squint-induced modifications of callosal connections in cats. Brain Res 144: 169–172Google Scholar
  26. Merzenich MM, Jenkins WM, Middlebrooks JC (1984) Observations and organisational features of the central auditory nervous systems. In: Edelman GM, Gall WE, Cowan WM (eds) Dynamical aspects of neocortical function. Wiley, New York, pp 397–424Google Scholar
  27. Mitchell DE (1980) Sensitive periods in visual development. In: Aslin RN, Alberts JR, Petersen MR (eds) Development of perception, vol II. Academic Press, New York, pp 3–43Google Scholar
  28. Nieuwkoop PD, Faber J (1967) A normal table of Xenopus laevis (Daudin), 2nd edn. North-Holland, AmsterdamGoogle Scholar
  29. Olson CR, Freeman RD (1978) Development of eye alignment in cats. Nature 271: 446–447Google Scholar
  30. Pettigrew JD (1974) The effect of visual experience on the development of stimulus specificity by kitten cortical neurones. J Physiol (Lond) 237: 49–74Google Scholar
  31. Pettigrew JD (1978) The paradox of the critical period for striate cortex. In: Cotman LW (ed) Neuronal plasticity. Raven Press, New York, pp 311–330Google Scholar
  32. Riley JN, Marchand ER (1979) Improvements in the benzidine dihydrochloride horseradish peroxidase method. Stain Technol 53: 290–291Google Scholar
  33. Schmidt JT, Eisele LE (1985) Stroboscopic illumination and darkrearing block the sharpening of the regenerated retinotectal map in goldfish. Brain Res 269: 29–39Google Scholar
  34. Sherman JM (1972) Development of interocular alignment in cats. Brain Res 37: 187–203Google Scholar
  35. Shlaer R (1971) Shift in binocular disparity causes compensatory change in the cortical structure of kittens. Science 173: 638–641Google Scholar
  36. Udin SB, Keating MJ (1981) Plasticity in a central nervous pathway in Xenopus: anatomical changes in the isthmo-tectal projection after larval eye rotation. J Comp Neurol 203: 575–594Google Scholar
  37. Witkovsky P, Gallin E, Hollyfield JG, Ripps H, Bridges CDB (1976) Photoreceptor thresholds and visual pigment levels in normal and vitamin A-deprived Xenopus laevis. J Neurophysiol 39: 1272–1287Google Scholar

Copyright information

© Springer-Verlag 1989

Authors and Affiliations

  • S. Grant
    • 1
  • M. J. Keating
    • 1
  1. 1.Division of Neurophysiology and NeuropharmacologyNational Institute for Medical ResearchLondonUK

Personalised recommendations