Skip to main content
Log in

Synaptic architecture of glomeruli in superficial dorsal horn of rat spinal cord, as shown in serial reconstructions

  • Published:
Journal of Neurocytology

Summary

Using serial section EM analysis, synaptic organization of glomeruli in lamina II of the dorsal horn of the rat has been examined. Four CI-terminals (small, dark and sinuous), four CIIa (large, light and regular, without neurofilaments) and four CIIb, (with neurofilaments) at the centres of synaptic glomeruli of types I, IIa and IIb, respectively, were serially sectioned and reconstructed. Asymmetrical synapses between the central terminal (C) and dendritic profiles without synaptic vesicles (D) prevailed in all types of glomeruli. Symmetrical dendroaxonic contacts with presynaptic dendrites (V1 → C) occurred practically only in type I glomeruli in which there were also more asymmetrical C → V1 contacts than in type II glomeruli. Symmetrical axoaxonic synapses V2 → C were more abundant in type IIa and IIb glomeruli. Type IIa glomeruli had a significantly larger number of C → D synapses and of all synapses per unit area of C surface, than type IIb glomeruli.

Triadic systems with C and D postsynaptic to V2 were nearly as numerous as those involving V1 in type I glomeruli. Triads with V2 were however largely preponderant in type IIa and virtually exclusive in type IIb. It thus seems that each of the three types of glomerulus has its own pattern of synaptic interactions which might reflect specific complexes of feed-forward and feed-back mechanisms. In type I glomeruli, excitation of second-order neurons by nociceptive CI terminals may be controlled in similar proportions by presynaptic dendrites excited within the glomerulus by the C terminal itself, or by peripheral axons excited from outside the glomerulus. This kind of control is likely to prevail in type IIa glomeruli and to be the only efficient modulatory mechanism in type IIb glomeruli.

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

  • Barber, R. P., Vaughn, J. E., Saito, K., Mclaughlin, B. J. &Roberts, E. (1978) GABAergic terminals are presynaptic to primary afferent terminals in the substantia gelatinosa of the rat spinal cord.Brain Research 141, 35–55.

    PubMed  Google Scholar 

  • Beal, J. A. &Fox, C. A. (1976) Afferent fibers in the substantia gelatinosa of the adult monkey (Macaca mulatta): a Golgi study.Journal of Comparative Neurology 168, 113–44.

    PubMed  Google Scholar 

  • Bennett, G. J., Ruda, M. A., Gobel, S. &Dubner, R. (1982) Enkephalin immunoreactive stalked cells and lamina IIb islet cells in cat substantia gelatinosa.Brain Research 240, 162–6.

    PubMed  Google Scholar 

  • Blackstad, T. W., Heimer, L. &Mugnaini, E. (1981) Experimental neuroanatomy. General approaches and laboratory procedures. InNeuroanatomical Tract-Tracing Methods (edited byHeimer, L. andRobards, M. J.), pp. 1–53. New York: Plenum Press.

    Google Scholar 

  • Coimbra, A., Ribeiro-Da-Silva, A. &Pignatelli, D. (1984) Effects of dorsal rhizotomy on the several types of primary afferent terminals in laminae I-III of the rat spinal cord. An electron microscope study.Anatomy and Embryology 170, 279–87.

    PubMed  Google Scholar 

  • Coimbra, A., Sodré-Borges, B. P. &Magalhães, M. M. (1974) The substantia gelatinosa Rolandi of the rat. Fine structure, cytochemistry (acid phosphatase) and changes after dorsal root section.Journal of Neurocytology 3, 199–217.

    PubMed  Google Scholar 

  • Duncan, D. &Morales, R. (1978) Relative numbers of several types of synaptic connections in the substantia gelatinosa of the cat spinal cord.Journal of Comparative Neurology 182, 601–10.

    PubMed  Google Scholar 

  • Gobel, S. (1974) Synaptic organization of the substantia gelatinosa glomeruli in the spinal trigeminal nucleus of the adult cat.Journal of Neurocytology 3, 219–43.

    PubMed  Google Scholar 

  • Gobel, S. (1976) Dendroaxonic synapses in the substantia gelatinosa glomeruli of the spinal trigeminal nucleus of the cat.Journal of Comparative Neurology 167, 165–76.

    PubMed  Google Scholar 

  • Gobel, S., Falls, W. M., Bennett, G. J., Abdelmoumene, M., Hayashi, H. &Humphrey, E. (1980) An EM analysis of the synaptic connections of horseradish peroxidase-filled stalked cells and islet cells in the substantia gelatinosa of adult cat spinal cord.Journal of Comparative Neurology 194, 781–807.

    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 

  • Hámori, J., Pasik, T., Pasik, P. &Szentágothai, J. (1974) Triadic synaptic arrangements and their possible significance in the lateral geniculate nucleus of the monkey.Brain Research 80, 379–93.

    PubMed  Google Scholar 

  • Knyihár-Csillik, E., Csillik, B. &Rakic, P. (1982a) Ultrastructure of normal and degenerating glomerular terminals of dorsal root axons in the substantia gelatinosa of the rhesus monkey.Journal of Comparative Neurology 210, 357–75.

    Google Scholar 

  • Knyihàr-Csillik, E., Csillik, B. &Rakic, P. (1982b) Periterminal synaptology of dorsal root glomerular terminals in the substantia gelatinosa of the spinal cord in the rhesus monkey.Journal of Comparative Neurology 210, 376–99.

    PubMed  Google Scholar 

  • Murray, M., Battisti, W. &Goldberger, M. E. (1983) Synaptic replacement in deafferented dorsal horn (lamina II) of cat.Neuroscience Abstracts 9, 987.

    Google Scholar 

  • Nagy, J. I., Hunt, S. P., Iversen, L. L. &Emson, P. C. (1981) Biochemical and anatomical observations on the degeneration of peptide-containing primary afferent neurons after neonatal capsaicin.Neuroscience 6, 1923–34.

    PubMed  Google Scholar 

  • Palay, S. L. &Chan-Palay, V. (1974)Cerebellar Cortex. Cytology and Organization. New York: Springer-Verlag.

    Google Scholar 

  • Peachey, L. D. (1958) Thin sections: 1. A study of section thickness and physical distortion produced during microtomy.Journal of Biophysical and Biochemical Cytology 4, 233–42.

    PubMed  Google Scholar 

  • Ralston, III, H. J. (1979a) Neuronal circuitry of the ventrobasal thalamus: The role of presynaptic dendrites. InThe Neurosciences: Fourth Study Program (edited bySchmitt, F. O. andWorden, F. G.), pp. 373–9. Cambridge, Massachusetts, London: MIT Press.

    Google Scholar 

  • Ralston, III, H. J. (1979b) The fine structure of laminae I, II and III of the macaque spinal cord.Journal of Comparative Neurology 184, 619–42.

    Google Scholar 

  • Ralston, III, H. J. &Ralston, D. D. (1979) The distribution of dorsal root axons in laminae I, II and III of the macaque spinal cord: A quantitative electron microscope study.Journal of Comparative Neurology 184, 643–84.

    PubMed  Google Scholar 

  • Réthelyi, M. (1977) Preterminal and terminal axon arborizations in the substantia gelatinosa of cat's spinal cord.Journal of Comparative Neurology 172, 511–28.

    PubMed  Google Scholar 

  • Réthelyi, M. &Szentágothai, J. (1969) The large synaptic complexes of the substantia gelatinosa.Experimental Brain Research 7, 258–74.

    Google Scholar 

  • Ribeiro-Da-Silva, A. &Coimbra, A. (1980) Neuronal uptake of [3H]Gaba and [3H]glycine in laminae I-III (substantia gelatinosa Rolandi) of the rat spinal cord. An autoradiographic study.Brain Research 188, 449–64.

    PubMed  Google Scholar 

  • Ribeiro-Da-Silva, A. &Coimbra, A. (1982) Two types of synaptic glomeruli and their distribution in laminae I-III of the rat spinal cord.Journal of Comparative Neurology 209, 176–86.

    Google Scholar 

  • Ribeiro-Da-Silva, A. &Coimbra, A. (1984) Capsaicin causes selective damage to type I synaptic glomeruli in rat substantia gelatinosa.Brain Research 290, 380–3.

    PubMed  Google Scholar 

  • Ribeiro-Da-Silva, A., Pignatelli, D. &Coimbra, A. (1980) Fine structural distribution of [3H]glycine uptake by the neuropil in the substantia gelatinosa Rolandi of the rat.Ciência Biológiea (Portugal) 5, 35a.

    Google Scholar 

  • Ribeiro-Da-Silva, A., Pignatelli, D. &Coimbra, A. (1983) Three types of synaptic glomeruli in the rat substantia gelatinosa Rolandi, as shown in reconstructions from ultrathin sections.Neuroscience Letters Suppl. 14, S307.

    Google Scholar 

  • Snyder, R. L. (1982) Light and electron microscope autoradiographic study of the dorsal root projections to the cat dorsal horn.Neuroscience 7, 1417–37.

    PubMed  Google Scholar 

  • Spacek, J. &Lieberman, A. R. (1974) Ultrastructure and three-dimensional organization of synaptic glomeruli in rat somatosensory thalamus.Journal of Anatomy 117, 487–516.

    PubMed  Google Scholar 

  • Weibel, E. R. (1973) Stereological techniques for electron microscopic morphometry. InPrinciples and Techniques of Electron Microscopy. Biological Applications, Vol. 3 (edited byHayat, M. A.), pp. 237–96. New York: Van Nostrand Reinhold Company.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ribeiro-Da-Silva, A., Pignatelli, D. & Coimbra, A. Synaptic architecture of glomeruli in superficial dorsal horn of rat spinal cord, as shown in serial reconstructions. J Neurocytol 14, 203–220 (1985). https://doi.org/10.1007/BF01258448

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01258448

Keywords

Navigation