Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Golgi type II interneurons in the neuronal circuit of the monkey lateral geniculate nucleus

  • 55 Accesses

  • 90 Citations

Summary

Total excision of areas 17-18-19 in the monkey leads to disappearance of relay cells and corticogeniculate axon terminals in the LGN (lateral geniculate nucleus). The few remaining neurons can be safely considered as Golgi type II cells. Electron microscopic examination of such material revealed small ovoid neurons and synaptic clusters encapsulated by glia. Within the cluster there were the characteristic axon terminal of retinal origin, and a peculiar light and large profile with features of both axons (small, flattened synaptic vesicles) and dendrites (many microtubules, endoplasmic cisterns and free ribosomes) in varying proportions. These elements were also present within the heavily gliotic general neuropil and, in longitudinal section, showed segments with strongly dendritic features, and others with vesicles either scattered or grouped near synaptic specializations. Similar profiles were also seen in normal LGN. Light microscopic examination of Golgi series from adult normal monkeys revealed two types of interneurons in the LGN, both having extremely thin axons which could not correspond in size to the ambiguous profiles described above. The latter could well match the appendages so frequently shown by the dendrites of one of the interneuron types. These findings suggest that the synapses in the glomeruli of LGN previously defined as “axo-axonic” may in fact be between optic axon terminals and the dendritic profiles with synaptic vesicles delineated in this study. Thence, the role of the Golgi type II interneuron could be interpreted at least in part as lateral inhibition.

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

References

  1. Andersen, P., Eccles, J.C., Sears, T.A.: The ventro-basal complex of the thalamus: Types of cells, their responses and their functional organization. J. Physiol. (Lond.) 174, 370–399 (1964).

  2. Colonnier, M., Guillery, R.W.: Synaptic organization in the lateral geniculate nucleus of the monkey. Z. Zellforsch. 62, 333–355 (1964).

  3. Dowling, J.E., Boycott, B.B.: Organization of the primate retina: electron microscopy. Proc. roy. Soc. B. 166, 80–111 (1966).

  4. Famiglietti, E.V.: Dendro-dendritic synapses in the lateral geniculate nucleus of the cat. Brain Res. 20, 181–191 (1970).

  5. Guillery, R.W.: A study of Golgi preparations from the dorsal lateral geniculate nucleus of the adult cat. J. comp. Neurol. 128, 21–50 (1966).

  6. —: The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus of the cat. Z. Zellforsch. 96, 1–38 (1969).

  7. —, Colonnier, M.: Synaptic patterns in the dorsal lateral geniculate nucleus of the monkey. Z. Zellforsch. 103, 90–108 (1970).

  8. Hámori, J.: Presynaptic-to-presynaptic axon contacts under experimental conditions giving rise to rearrangement of synaptic structures. In: Structure and Function of Inhibitory Neuronal Mechanisms, pp. 71–80. Ed. by C. von Euler, S. Skoglund and U. Söderberg. Proceedings of the Fourth International Meeting of Neurobiologists, Stockholm, Sept. 1966. Oxford: Pergamon Press 1968.

  9. Jones, E.G., Powell, T.P.S.: Electron microscopy of synaptic glomeruli in the thalamic relay nuclei of the cat. Proc. roy. Soc. B. 172, 153–171 (1969).

  10. Karnowski, M.J.: A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J. Cell Biol. 27, 137A-138A (1965).

  11. Le Vay, S.: On the neurons and synapses of the lateral geniculate nucleus of the monkey, and the effects of eye enucleation. Z. Zellforsch. 113, 396–419 (1971).

  12. Majorossy, K., Réthelyi, M.: Synaptic architecture in the medial geniculate body (ventral division). Exp. Brain Res. 6, 306–323 (1968).

  13. Morest, D.K.: The neuronal architecture of the medial geniculate body of the cat. J. Anat. (Lond.) 98, 611–630 (1964).

  14. —: The laminar structure of the medial geniculate body of the cat. J. Anat. (Lond.) 99, 143–160 (1965).

  15. —: Dendrodendritic synapses of cells that have axons: The fine structure of the Golgi type II cell in the medial geniculate body of the cat. Z. Anat. Entwickl.-Gesch. 133, 216–246 (1971).

  16. Pasik, P., Pasik, T., Schilder, P.: Extrageniculostriate vision in the monkey: Discrimination of luminous flux-equated figures. Exp. Neurol. 24, 421–437 (1969).

  17. Pasik, T., Pasik, P.: The visual world of monkeys deprived of striate cortex: effective stimulus parameters and the importance of the accessory optic system. In: Visual Processes in Vertebrates. Ed. by T. Shipley and J.E. Dowling. Vision Res. Suppl. No. 3, pp. 419–435. Oxford: Pergamon Press 1971.

  18. Pecci-Saavedra, J., Vaccarezza, O.L.: Synaptic organization of the glomerular complexes in the lateral geniculate nucleus of Cebus monkey. Brain Res. 8, 389–393 (1968).

  19. Peters, A., Palay, S.L.: The morphology of laminae A and A1 of the dorsal nucleus of the lateral geniculate body of the cat. J. Anat. (Lond.) 100, 451–486 (1966).

  20. Polyak, S.: The Vertebrate Visual System. Ed. by H. Kluver, p. 404. Chicago: Chicago Univ. Press 1957.

  21. Rámon y Cajal, S.: Histologie des Système Nerveux de l'Homme et des Vertébrés, Tome II. Paris: Maloine 1911.

  22. Rall, W., Shepherd, G.M., Reese, T.S., Brightman, M.W.: Dendro-dendritic synaptic pathway for inhibition in the olfactory bulb. Exp. Neurol. 14, 44–56 (1966).

  23. Ralston, H.J., Herman, M.M.: The fine structure of neurons and synapses in the ventro-basal thalamus of the cat. Brain Res. 14, 77–97 (1969).

  24. Sanderson, K.J., Bishop, P.O., Darian-Smith, I.: The properties of the binocular fields of lateral geniculate nucleus. Exp. Brain Res. 13, 178–207 (1971).

  25. Schilder, P., Pasik, T., Pasik, P.: Extrageniculostriate vision in the monkey. II. Demonstration of brightness discrimination. Brain Res. 32, 383–398 (1971).

  26. Singer, W., Pöppel, E., Creutzfeldt, O.: Inhibitory interaction in the cat's lateral geniculate nucleus. Exp. Brain Res. 14, 210–226 (1972).

  27. Szentágothai, J.: The structure of the synapse in the lateral geniculate body. Acta anat. (Basel) 55, 166–185 (1963).

  28. - Anatomical aspects of junctional transformation. In: Information Processing in the Nervous System, vol. 3. pp. 119–136. Ed. by R.W. Gerard and J.W. Duyff. Proceedings of the International Union of Physiological Sciences. XXII. International Congress Leiden, 1962. Excerpta Medica Congress Sr. 49. Amsterdam, 1964.

  29. —: Models of specific neuron arrays in thalamic relay nuclei. Acta morph. Acad. Sci. hung. 15, 113–124 (1967).

  30. —: Glomerular synapses, complex synaptic arrangements and their operational significance. In: The Neurosciences: Second Study Program, pp. 427–443. Editor-in-chief: F.O. Schmitt. New York: The Rockefeller University Press 1970.

  31. —: Hámori, J., Tömböl, T.: Degeneration and electron microscope analysis of the synaptic glomeruli in the lateral geniculate body. Exp. Brain Res. 2, 283–301 (1966).

  32. —: Growth and differentiation of synaptic structures under circumstances of deprivation of function and of distant connections. In: Cellular Dynamics of the Neuron, pp. 301–320. Ed. by S.H. Barondes. New York-London: Academic Press 1969.

  33. Tello, F.: Disposicion macroscopica y estructura del cuerpo geniculado externo. Trab. Lab. Invest. Biol. Univ. Madrid. 3, 39–62 (1904).

  34. Tömböl, T.: Short neurons and their synaptic relations in the specific thalamic nuclei. Brain Res. 3, 307–326 (1966/1967).

  35. —: Terminal arborizations in specific afferents in the specific thalamic nuclei. Acta morph. Acad. Sci. hung. 17, 273–284 (1969a).

  36. —: Two types of short axon (Golgi 2nd) interneurons in the specific thalamic nuclei. Acta morph. Acad. Sci. hung. 17, 285–297 (1969b).

  37. Wong, M.T.T.: Somato-dendritic and dendro-dendritic synapses in the squirrel monkey lateral geniculate nucleus. Brain Res. 20, 135–139 (1970).

Download references

Author information

Additional information

This research was supported in part by U.S.P.H.S. Grants MH-02261 and K3-EY-16, 865. The technical assistance of Mr. David Kahn and Miss Rosemary Lang is gratefully acknowledged.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Pasik, P., Pasik, T., Hámori, J. et al. Golgi type II interneurons in the neuronal circuit of the monkey lateral geniculate nucleus. Exp Brain Res 17, 18–34 (1973). https://doi.org/10.1007/BF00234561

Download citation

Key words

  • Lateral geniculate nucleus
  • Monkeys
  • Golgi type II interneurons
  • Synaptic arrangements