Skip to main content
Log in

The formation and maturation of synapses in the visual cortex of the rat. I. Qualitative analysis

  • Published:
Journal of Neurocytology

Summary

Synapse formation and maturation were examined in the visual cortex of albino rats from birth to maturity. During the first few days of postnatal life, synapses were sparsely scattered in the subplate zone and in layer I. They appeared immature as judged by the irregular shapes of the presynaptic and postsynaptic profiles, the relatively poorly defined membrane specializations and the presence of only a few synaptic vesicles in the presynaptic structures. As the neuropil matured, synapses were observed throughout the cortex, showing increased thickening of the membrane specializations and more vesicles. However, it was not until the end of the fourth postnatal week that they appeared qualitatively indistinguishable from synapses identified in the adult material.

A feature characteristic of the developing visual cortex was the presence of vacant membrane specializations that resembled type I postsynaptic densities. These specializations, which were located either opposite extracellular space or opposite another neuronal process, were only evident during the initial stages of synaptogenesis and their frequency decreased as the number of synapses increased. In addition, transitional forms between these densities and true type I synapses were identified during the first two postnatal weeks. Structures that resembled vacant postsynaptic densities typical of type II synapses were not observed. The earliest identified forms of type II synaptic contacts identified consisted of two profiles that exhibited symmetrical membrane specializations and cleft material. Based on these observations, a scheme has been proposed for the formation of type I and type II synapses in the visual cortex of the rat.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adinolfi, A. M. (1972) Morphogenesis of synaptic junctions in layers I and II of the somatic sensory cortex.Experimental Neurology 34, 372–82.

    Google Scholar 

  • Aghajanian, G. K. &Bloom, F. E. (1967) The formation of synaptic junctions in developing rat brain: A quantitative electron microscopic study.Brain Research 6, 716–27.

    Google Scholar 

  • Altman, J. (1971) Coated vesicles and synaptogenesis. A developmental study in the cerebellar cortex of the rat.Brain Research 30, 311–22.

    Google Scholar 

  • Berry, M. (1974) Development of the cerebral neocortex of the rat. InStudies on the Development of Behavior and the Nervous System, Vol. 2, Aspects of Neurogenesis (edited byGottlieb, G.), pp. 7–67. New York: Academic Press.

    Google Scholar 

  • Blue, M. E. &Parnavelas, J. G. (1983) The formation and maturation of synapses in the visual cortex of the rat. II. Quantitative analysis.Journal of Neurocytology 12, 697–712.

    Google Scholar 

  • Brightman, M. W. &Reese, T. S. (1969) Junctions between intimately apposed cell membranes in the vertebrate brain.Journal of Cell Biology 40, 648–77.

    Google Scholar 

  • Cajal, S. Ramón (1960)Studies on Vertebrate Neurogenesis (translated byGuth, L.). Springfield, Illinois: Charles C. Thomas.

    Google Scholar 

  • Caley, D. W. &Maxwell, D. S. (1968) An electron microscopic study of neurons during postnatal development of the rat cerebral cortex.Journal of Comparative Neurology 133, 17–44.

    Google Scholar 

  • Connors, B. W., Benard, I. S. &Prince, D. A. (1983) Coupling between neurons in the developing rat neocortex.Journal of Neuroscience (in press).

  • Cragg, B. G. (1972) The development of synapses in cat visual cortex.Investigative Ophthalmology 11, 377–85.

    Google Scholar 

  • Gray, E. G. (1959) Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron microscope study.Journal of Anatomy 93, 420–33.

    Google Scholar 

  • Hayes, B. P. &Roberts, A. (1973) Synaptic junction development in the spinal cord of an amphibian embryo: an electron microscope study.Zeitschrift für Zellforschung und mikroskopische Anatomie 137, 251–69.

    Google Scholar 

  • Hayes, B. P. &Roberts, A. (1974) The distribution of synapses along the spinal cord of an amphibian embryo: an electron microscope study of junction development.Cell and Tissue Research 153, 227–44.

    Google Scholar 

  • Hinds, J. W. &Hinds, P. L. (1976) Synapse formation in the mouse olfactory bulb. II. Morphogenesis.Journal of Comparative Neurology 169, 41–62.

    Google Scholar 

  • Jacobson, M. (1978)Developmental Neurobiology 2nd edn. New York, London: Plenum Press.

    Google Scholar 

  • Johnson, R. &Armstrong-James, M. (1970) Morphology of superficial postnatal cerebral cortex with special reference to synapses.Zeitschrift für Zellforschung und mikroskopische Anatomie 110, 540–58.

    Google Scholar 

  • Juraska, J. M. &FifkovÁ, E. (1979) An electron microscope study of the early postnatal development of the visual cortex of the hooded rat.Journal of Comparative Neurology 183, 257–68.

    Google Scholar 

  • König, N., Roch, G. &Marty, R. (1975) The onset of synaptogenesis in rat temporal cortex.Anatomy and Embryology 148, 73–87.

    Google Scholar 

  • Krieg, W. J. S. (1946) Connections of the cerebral cortex. I. The albino rat. A. Topography of the cortical areas.Journal of Comparative Neurology 84, 221–76.

    Google Scholar 

  • Kristt, D. A. &Molliver, M. E. (1976) Synapses in newborn rat cerebral cortex: a quantitative ultrastructural study.Brain Research 108, 180–6.

    Google Scholar 

  • Larramendi, L. M. H. (1969) Analysis of synaptogenesis in the cerebellum of the mouse. InNeurobiology of Cerebellar Evolution and Development (edited byLlinas, R.), pp. 803–43. Chicago: American Medical Association.

    Google Scholar 

  • McGraw, C. F. &McLaughlin, B. J. (1980) Fine structural studies of synaptogenesis in the superficial layers of chick optic tectum.Journal of Neurocytology 9, 79–93.

    Google Scholar 

  • Miller, M. (1981) Maturation of rat visual cortex. I. A quantitative study of Golgi-impregnated pyramidal neurons.Journal of Neurocytology 10, 859–78.

    Google Scholar 

  • Miller, M. &Peters, A. (1981) Maturation of rat visual cortex. II. A combined Golgi-electron microscope study of pyramidal neurons.Journal of Comparative Neurology 203, 555–73.

    Google Scholar 

  • Molliver, M. E., Kostović, I. &Van Der Loos, H. (1973) The development of synapses in cerebral cortex of the human fetus.Brain Research 50, 403–7.

    Google Scholar 

  • Molliver, M. E. &Van Der Loos, H. (1970) The ontogenesis of cortical circuitry: the spatial distribution of synapses in somesthetic cortex of newborn dog.Ergebnisse der Anatomie und Entwicklungsgeschichte 42, 1–54.

    Google Scholar 

  • Ochi, J. (1967) Elektronenmikroskopische Untersuchung des bulbus olfactorius der Ratte während der entwicklung.Zeitschrift für Zellforschung und mikroskopische Anatomie 76, 339–48.

    Google Scholar 

  • Oppenheim, R. W., Chu-Wang, I. -W. &Foelix, R. F. (1975) Some aspects of synaptogenesis in the spinal cord of the chick embryo: a quantitative electron microscopic study.Journal of Comparative Neurology 161, 383–418.

    Google Scholar 

  • Parnavelas, J. G., Bradford, R., Mounty, E. J. &Lieberman, A. R. (1978) The development of non-pyramidal neurons in the visual cortex of the rat.Anatomy and Embryology 155, 1–14.

    Google Scholar 

  • Parnavelas, J. G. &Globus, A. (1976) The effect of continuous illumination on the development of cortical neurons in the rat: a Golgi study.Experimental Neurology 51, 637–47.

    Google Scholar 

  • Parnavelas, J. G. &Lieberman, A. R. (1979) An ultrastructural study of the maturation of neuronal somata in the visual cortex of the rat.Anatomy and Embryology 157, 311–28.

    Google Scholar 

  • Parnavelas, J. G., Lieberman, A. R. &Webster, K. E. (1977a) Organization of neurons in the visual cortex, area 17, of the rat.Journal of Anatomy 124, 305–22.

    Google Scholar 

  • Parnavelas, J. G., Sullivan, K., Lieberman, A. R. &Webster, K. E. (1977b) Neurons and their synaptic organization in the visual cortex of the rat. Electron microscopy of Golgi preparations.Cell and Tissue Research 183, 499–517.

    Google Scholar 

  • Peters, A. (1970) The fixation of central nervous tissue and the analysis of electron micrographs of the neuropil, with special reference to the cerebral cortex. InContemporary Research Methods in Neuroanatomy (edited byNauta, W. J. H. andEbbesson, S. O. E.), pp. 56–76. New York, Heidelberg, Berlin: Springer-Verlag.

    Google Scholar 

  • Peters, A. &FairÉn, A. (1978) Smooth and sparsely spined stellate cells in the visual cortex of the rat: a study using a combined Golgi-electron microscope technique.Journal of Comparative Neurology 181, 129–72.

    Google Scholar 

  • Peters, A. &Kaiserman-Abramof, I. R. (1970) The small pyramidal neuron of the rat cerebral cortex. The perikaryon, dendrites and spines.American Journal of Anatomy 127, 321–55.

    Google Scholar 

  • Peters, A., Palay, S. L. &Webster, H. De F. (1976)The Fine Structure of the Nervous System: The Neurons and Supporting Cells. Philadelphia: W. B. Saunders.

    Google Scholar 

  • Rees, R. P. (1978a) Structure of cell coats during initial stages of synapse formation on isolated cultured sympathetic neurons.Journal of Neurocytology 7, 679–91.

    Google Scholar 

  • Rees, R. P. (1978b) The morphology of interneuronal synaptogenesis: a review.Federation Proceedings 37, 2000–9.

    Google Scholar 

  • Rees, R. P., Bunge, M. B. &Bunge, R. P. (1976) Morphological changes in the neuritic growth cone and target neuron during synaptic junction development in culture.Journal of Cell Biology 68, 240–63.

    Google Scholar 

  • Rice, F. L. &Van Der Loos, H. (1977) Development of the barrels and barrel field in the somatosensory cortex of the mouse.Journal of Comparative Neurology 171, 545–60.

    Google Scholar 

  • Sarkisov, S. A., Popova, E. N. &Bogolepov, N. N. (1966) Structure of synapses in evolutionary aspect (optic and electron microscopic studies). InEvolution of the Forebrain (edited byHassler, R. andStephan, H.), pp. 225–36. Stuttgart: Georg Thieme Verlag.

    Google Scholar 

  • Sloper, J. J. &Powell, T. P. S. (1978) Gap junctions between dendrites and somata of neurons in the primate sensori-motor cortex.Proceedings of the Royal Society of London B 203, 39–47.

    Google Scholar 

  • Stelzner, D. J., Martin, A. H. &Scott, G. L. (1973) Early stages of synaptogenesis in the cervical spinal cord of the chick embryo.Zeitschrift für Zellforschung und mikroskopische Anatomie 138, 475–88.

    Google Scholar 

  • Tennyson, V. M. (1970) The fine structure of the axon and growth cone of the dorsal root neuroblast of the rabbit embryo.Journal of Cell Biology 44, 62–79.

    Google Scholar 

  • Vrensen, G., De Groot, D. &Nunes-Cardozo, J. (1977) Postnatal development of neurons and synapses in the visual and motor cortex of rabbits: a quantitative light and electron microscopic study.Brain Research Bulletin 2, 405–16.

    Google Scholar 

  • Westrum, L. E. (1975) Electron microscopy of synaptic structures in olfactory cortex of early postnatal rats.Journal of Neurocytology 4, 713–32.

    Google Scholar 

  • Westrum, L. E., Hugh Jones, D., Gray, E. G. &Barron, J. (1980) Microtubules, dendritic spines and spine apparatuses.Cell and Tissue Research 208, 171–81.

    Google Scholar 

  • Wolff, J. R. (1978) Ontogenetic aspects of cortical architecture: lamination. InArchitectonics of the Cerebral Cortex (edited byBrazier, M. A. B. andPetsche, H.), pp. 159–73. New York: Raven Press.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Blue, M.E., Parnavelas, J.G. The formation and maturation of synapses in the visual cortex of the rat. I. Qualitative analysis. J Neurocytol 12, 599–616 (1983). https://doi.org/10.1007/BF01181526

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01181526

Keywords

Navigation