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Axosomatic synapses in the visual cortex of adult rat. A comparison between GABA-accumulating and other neurons

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Journal of Neurocytology

Summary

Differences in axosomatic synapses between GABA-accumulating [G(+)N] or non-accumulating [G(−)N] neurons have been investigated in the visual cortex of adult rat. The neurons were classified and localized in light microscopic autoradiograms after [3H]GABA injections. The cells were then resectioned for electron microscopic identification of type 1 synapses (T1S) and type 2 synapses (T2S). A total of 167 neurons [45 G(+)N, 122 G(−)N] situated in laminae II-VI were evaluated. The two groups of neurons were not uniform populations. G(−)N included both pyramidal and non-pyramidal neurons, whereas no typical pyramidal neurons were found among G(+)N.

A total of 691 synaptic contacts was evaluated for these groups of somata. The density of synapses was higher on G(+)N than on G(−)N. This was mainly due to a difference in the number of T1S. On G(−)N the frequency distributions of both types of synapses represented Poisson distributions, indicating that there were stochastic variations around mean values. In contrast, on G(+)N the distribution was exponential which suggests that G(+)N include several subpopulations with different densities of T1S.

On all cortical neurons the average density of T2S was 50–60 T2S per 1000 μm2 of soma surface, which resembles the density in the neuropil. In contrast, T1S varied from zero to a mean of 12 per 1000 μm2 on G(−)N and to a mean of 51 per 1000 μm2 on G(+)N, i.e. the density of T1S, unlike T2S, is much smaller on neuronal somata than in the surrounding neuropil. It is suggested that the formation of axosomatic T1S, but not of T2S, is suppressed to a variable degree on almost all cortical neurons. Only on pyramidal neurons does the suppression of T1S seem to be complete.

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References

  • Akert, K., Pfenninger, K., Sandri, C. &Moor, H. (1972) Freeze etching and cytochemistry of vesicles and membrane complexes in synapses of the central nervous system. InStructure and Function of Synapses (edited byPappas, G. D. &Purpura, D. P.), pp. 67–86. New York: Raven Press.

    Google Scholar 

  • Bär, Th. (1977) Wirkung chronischer Hypoxie auf die postnatale Synaptogenese im Occipitalcortex der Ratte.Verhandlungen der Anatomischen Gesellschaft 71, 915–24.

    PubMed  Google Scholar 

  • Baughman, R. W. &Bilbert, C. D. (1981) Aspartate and glutamate as possible neurotransmitters in the visual cortex.Journal of Neuroscience 1, 427–39.

    PubMed  Google Scholar 

  • Bodian, D. (1970) An electron microscopical characterization of classes of synaptic vesicles by means of controlled aldehyde fixation.Journal of Cell Biology 44, 115–24.

    PubMed  Google Scholar 

  • Chronwall, B. M. &Wolff, J. R. (1978) Classification and location of neurons taking up [3H]GABA in the visual cortex of rats. InAmino Acids as Chemical Transmitters (edited byFonnum, F.), pp. 297–303. New York: Plenum Publishing Corporation.

    Google Scholar 

  • Chronwall, B. &Wolff, J. R. (1980) Prenatal and postnatal development of GABA-accumulating cells in the occipital neocortex of rat.Journal of Comparative Neurology 190, 187–208.

    PubMed  Google Scholar 

  • Colonnier, M. (1968) Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study.Brain Research 9, 268–87.

    PubMed  Google Scholar 

  • Dubin, M. W. &Cleland, B. G. (1977) Organization of visual inputs to interneurons of lateral geniculate nucleus of the cat.Journal of Neurophysiology 40, 410–27.

    PubMed  Google Scholar 

  • Eccles, J. C. (1964)The Physiology of Synapses. Berlin, Göttingen, Heidelberg: Springer-Verlag.

    Google Scholar 

  • Gray, E. G. (1959) Axosomatic and axodendritic synapses of the cerebral cortex. An electron microscope study.Journal of Anatomy 93, 420–33.

    PubMed  Google Scholar 

  • Güldner, F. H. (1978) Synapses of optic nerve afferents in the rat suprachiasmatic nucleus. II. Structural variability as revealed by morphometric examination.Cell and Tissue Research 194, 37–54.

    PubMed  Google Scholar 

  • Güldner, F. H. &Wolff, J. R. (1978) Retinal afferents form Gray-type-I and type-II synapses in the suprachiasmatic nucleus (rat).Experimental Brain Research 32, 83–9.

    Google Scholar 

  • Hendry, S. H. C. &Jones, E. G. (1981) Sizes and distribution of intrinsic neurons incorporating tritiated GABA in monkey sensory-motor cortex.Journal of Neuroscience 1, 390–408.

    PubMed  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.

    PubMed  Google Scholar 

  • Hökfelt, T. &Ljungdahl, A. (1971) Uptake of [3H]noradrenaline and [3H]gamma-aminobutyric acid in isolated tissues of rat: an autoradiographic and fluorescence microscopic study.Progress in Brain Research 34, 87–102.

    Google Scholar 

  • Hökfelt, T. &Ljungdahl, A. (1972) Autoradiographic identification of cerebral and cerebellar cortical neurons accumulating labeled gamma-aminobutyric acid ([3H]GABA).Experimental Brain Research 14, 354–62.

    Google Scholar 

  • Jones, E. G. &Powell, T. P. S. (1970) Electron microscopy of the somatic sensory cortex of the cat. I. Cell types and synaptic organization.Philosophical Transactions of the Royal Society of London, Series B 257, 1–11.

    Google Scholar 

  • Joö, F., Dames, W. &Wolff, J. R. (1979) Effect of prolonged sodium bromide administration on the fine structure of dendrite in the superior cervical ganglion of adult rat.Progress in Brain Research 51, 109–15.

    PubMed  Google Scholar 

  • Kaplan, M. S. &Hinds, J. W. (1977) Neurogenesis in the adult rat: Electron microscopic analysis of light radioautographs.Science 197, 1092–4.

    PubMed  Google Scholar 

  • Larramendi, L. M. H., Fickenscher, L. &Lemkey-Johnston, N. (1967) Synaptic vesicles of inhibitory and excitatory terminals in the cerebellum.Science 156, 967–9.

    PubMed  Google Scholar 

  • Levay, S. (1973) Synaptic patterns in the visual cortex of the cat and monkey. Electron microscopy of Golgi preparations.Journal of Comparative Neurology 150, 53–86.

    PubMed  Google Scholar 

  • Mugnaini, E. (1970) The relation between cytogenesis and the formation of different types of synaptic contact.Brain Research 17, 169–79.

    PubMed  Google Scholar 

  • Palay, S. &Chan-Palay, V. (1974)Cerebellar cortex, pp. 333. Berlin, Heidelberg, New York: Springer-Verlag.

    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.

    PubMed  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.

    PubMed  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, 321–56.

    PubMed  Google Scholar 

  • Peters, A. &Fairen, 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.

    PubMed  Google Scholar 

  • Peters, A., Proskauer, C. C., Feldman, M. L. &Kimerer, L. (1979) The projection of the lateral geniculate nucleus to area 17 of the rat cerebral cortex. V. Degenerating axon terminals synapsing with Golgi impregnated neurons.Journal of Neurocytology 8, 331–57.

    PubMed  Google Scholar 

  • Ribak, C. E. (1978) Aspinous and sparsely-spinous stellate neurons in the visual cortex of rats contain glutamic acid decarboxylase.Journal of Neurocytology 7, 461–78.

    PubMed  Google Scholar 

  • Ribak, C. E., Vaughn, J. E. &Roberts, E. (1979) The GABA neurons and their axon terminals in rat corpus striatum as demonstrated by GAD immunocytochemistry.Journal of Comparative Neurology 187, 261–7.

    PubMed  Google Scholar 

  • Richardson, K. L., Jarett, L. &Finke, E. H. (1960) Embedding in epoxy resins for ultrathin sectioning in electron microscopy.Stain Technology 35, 313–23.

    PubMed  Google Scholar 

  • Sumner, B. E. H. (1975) A quantitative analysis of the response of presynaptic boutons to postsynaptic motor neuron axotomy.Experimental Neurology 46, 605–15.

    PubMed  Google Scholar 

  • Szentágothai, J. (1973) Synaptology of the visual cortex. InHandbook of Sensory Physiology Vol VII/3B (edited byJung, R.). Berlin, Heidelberg, New York: Springer-Verlag.

    Google Scholar 

  • Uchizono, K. (1965) Characteristics of excitatory and inhibitory synapses in the central nervous system of the cat.Nature 207, 642–3.

    PubMed  Google Scholar 

  • Uchizono, K. (1975)Excitation and inhibition. Synaptic Morphology. Tokyo: Igaku Shoin Ltd.

    Google Scholar 

  • Werner, L., Hedlich, A., Winkelmann, E. &Brauer, K. (1979) Versuch einer Identifizierung von Nervenzellen des visuellen Kortex der Ratte nach Nissl- und Golgi-Kopsch Darstellung.Journal für Hirnforschung 20, 121–39.

    Google Scholar 

  • White, E. L. (1978) Identified neurons in mouse SmI cortex which are postsynaptic to thalamocortical axon terminals: A combined Golgi-electron microscopic and degeneration study.Journal of Comparative Neurology 181, 627–62.

    PubMed  Google Scholar 

  • White, E. L. &Rock, M. P. (1980) Three-dimensional aspects and synaptic relationships of a Golgi-impregnated spiny stellate cell reconstructed from serial thin sections.Journal of Neurocytology 9, 615–36.

    Google Scholar 

  • Wolfe, J. R. (1976) Quantitative analysis of topography and development of synapses in the visual cortex.Experimental Brain Research Suppl.1, 259–63.

    Google Scholar 

  • Wolff, J. R. (1978) Ontogenetic aspects of cortical architecture: Lamination. InArchitectonics of the Cerebral Cortex (edited byBrazier, M. A. &Petsche, H.). New York: Raven Press.

    Google Scholar 

  • Wolff, J. R., Joö, F. &Dames, W. (1978) Plasticity in dendrites shown by continuous GABA administration in superior cervical ganglion of adult rat.Nature 274, 72–4.

    PubMed  Google Scholar 

  • Wolff, J. R., Joö, F., Dames, W. &Fehér, O. (1979) Induction and maintenance of free postsynaptic membrane thickenings in the adult superior cervical ganglion.Journal of Neurocytology 8, 549–63.

    PubMed  Google Scholar 

  • Wolfe, J. R., Joö, F., Dames, W. &Fehér, O. (1981) Neuroplasticity in the superior cervical ganglion as a consequence of long-lasting inhibition. InCellular Analogues of Conditioning and Neural Plasticity Advances in Physiological Science36, (edited byFehér, F. &Joö, F.). pp. 1–9. Oxford: Pergamon Press.

    Google Scholar 

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Wolff, J.R., Chronwall, B.M. Axosomatic synapses in the visual cortex of adult rat. A comparison between GABA-accumulating and other neurons. J Neurocytol 11, 409–425 (1982). https://doi.org/10.1007/BF01257986

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