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Periterminal synaptic organization of primary afferents in laminae I and IIo of the rat spinal cord, as shown after anterograde HRP labelling

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Journal of Neurocytology

Summary

The fine structure and periterminal synaptology of the primary afferent terminations in laminae I and IIo are examined in the rat, following anterograde labelling with horseradish peroxidase applied to the right C5-dorsal root. Labelled varicosities observed along the terminal arbors in parasagittal thick sections were relocated in ultrathin sections by electron microscopy. The labelled terminal profiles generated by the three primary afferent plexuses which can be identified by light microscopy in laminae I-IIo had similar fine structural features, except that axo-axonal contacts, although rare, were more frequent in the medial network plexus. Primary boutons were packed with agranular spherical vesicles and some large granular vesicles, and were mostly presynaptic to profiles of dendritic trunks of marginal cells. Unlabelled axonal profiles, either light with some flattened vesicles, or dense with round vesicles, were also presynaptic at symmetrical or asymmetrical contacts, respectively, to those dendritic profiles. It is suggested that such knobs of intrinsic origin are responsible for postsynaptic modulation of the primary noxious input. Although the 20 μm wide lamina IIo belongs cytoarchitectonically to lamina II and can be distinguished from lamina I by a decreased amount of myelinated fibres and large dendritic profiles, the periterminal synaptology was here found to be the same as in lamina I.

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References

  • Adams, J. C. (1981) Heavy metal intensification of DAB-based HRP reaction product.Journal of Histochemistry and Cytochemistry 29, 775.

    Google Scholar 

  • Beal, J. A. &Bicknell, H. R. (1981) Primary afferent distribution pattern in the marginal zone (lamina I) of adult monkey and cat lumbosacral spinal cord.Journal of Comparative Neurology 202, 255–63.

    Google Scholar 

  • Beattie, M. S., Bresnahan, J. C. &King, J. S. (1978) Ultrastructural identification of dorsal root primary afferent terminals after anterograde filling with horseradish peroxidase.Brain Research 153, 127–34.

    Google Scholar 

  • Bennett, G. J., Hayashi, H., Abdelmoumene, M. &Dubner, R. (1979) Physiological properties of stalked cells of the substantia gelatinosa intracellularly stained with horseradish peroxidase.Brain Research 164, 285–9.

    Google Scholar 

  • Bresnahan, J. C., Ho, R. H. &Beattie, M. S. (1984) A comparison of the ultrastructure of substance P and enkephalin-immunoreactive elements in the nucleus of the dorsal lateral funiculus and laminae I and II of the rat spinal cord.Journal of Comparative Neurology 229, 497–511.

    Google Scholar 

  • Brown, A. G. (1981) The organization of the dorsal horn. InOrganization in the Spinal Cord (edited byBrown, A. G.) pp. 136–53. Berlin, Heidelberg: Springer-Verlag.

    Google Scholar 

  • Carlton, S. M., McNeill, D. L., Chung, K. &Coggeshall, R. E. (1987) A light and electron microscope level analysis of calcitonin gene-related peptide (CGRP) in the spinal cord of the primate: an immunocytochemical study.Neuroscience Letters 82, 145–50.

    Google Scholar 

  • Carlton, S. M., McNeill, D. L., Chung, K. &Coggeshall, R. E. (1988) Organization of calcitonin generelated peptide-immunoreactive terminals in the primate dorsal horn.Journal Comparative of Neurology 276, 527–36.

    Google Scholar 

  • Cervero, F. &Iggo, A. (1980) The substantia gelatinosa of the spinal cord. A critical review.Brain 103, 717–72.

    Google Scholar 

  • Coimbra, A., Sodré-Borges, B. P. &Magalhäes, 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.

    Google Scholar 

  • Cruz, F., Lima, D. &Coimbra, A. (1987) Several morphological types of terminal arborizations of primary afferents in laminae I–II of the rat spinal cord, as shown after HRP labelling and Golgi impregnation.Journal of Comparative Neurology 261, 221–36.

    Google Scholar 

  • Cruz, F., Lima, D., Tavares, I. &Coimbra, A. (1990) Fine structure of the terminal arborizations of HRP labelled primary afferents projecting to laminae I-IIo.European Journal of Neuroscience Supplement3, S4242.

    Google Scholar 

  • Cruz, F., Lima, D., Zieglgänsberger, W. &Coimbra, A. (1991) Fine structure and synaptic architecture of HRP-labelled primary afferent terminations in lamina IIi of the rat dorsal horn.Journal of Comparative Neurology 305, 3–16.

    Google Scholar 

  • Difiglia, M., Arouin, N. &Leeman, S. E. (1982) Light microscopic and ultrastructural localization of immunoreactive substance P in dorsal horn of the monkey spinal cord.Neuroscience 7, 1127–39.

    Google Scholar 

  • Difiglia, M., Aronin, N. &Leeman, S. E. (1984) Ultrastructural localization of immunoreactive neurotensin in the monkey superficial dorsal horn.Journal of Comparative Neurology 225, 1–12.

    Google Scholar 

  • Glazer, E. J. &Basbaum, A. I. (1983) Opioid neurons and pain modulation: an ultrastructural analysis of enkephalin in cat superficial dorsal horn.Neuroscience 10, 357–76.

    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.

    Google Scholar 

  • Gobel, S. (1978) Golgi studies of the neurons in layer II of the dorsal horn of the medulla (trigeminal nucleus caudalis).Journal of Comparative Neurology 180, 395–414.

    Google Scholar 

  • Gobel, S. &Falls, W. M. (1979) Anatomical observations of horseradish peroxidase filled terminal primary axonal arborizations in layer II of the substantia gelatinosa of Rolando.Brain Research 175, 335–40.

    Google Scholar 

  • Gobel, S., Falls, W. M. &Humphrey, E. (1981) Morphology and synaptic connections of ultrafine primary axons in lamina I of the spinal dorsal horn: candidates for the terminal axonal arbors of primary neurons with unmyelinated (C) axons.Journal of Neuroscience 1, 1163–79.

    Google Scholar 

  • Gray, E. G. (1962) A morphological basis for pre-synaptic inhibition.Nature 193, 82–3.

    Google Scholar 

  • Honda, C. N., Rethelyi, M. &Petrusz, P. (1983) Preferential immunohistochemical localization of vasoreactive intestinal polypeptide in the sacral spinal cord of the cat: light and electron microscopic observations.Journal of Neuroscience 3, 2183–96.

    Google Scholar 

  • Hunt, S. P. &Rossi, J. (1985) Peptide- and non-peptide-containing unmyelinated primary afferents: the parallel processing of nociceptive information. InNociception and Pain (edited byIggo, A., Iversen, L. L. &Cervero, F.) pp. 283–9. London: The Royal Society.

    Google Scholar 

  • Kerr, F. W. L. (1970) The fine structure of the subnucleus caudalis of the trigeminal nerve.Brain Research 23, 129–45.

    Google Scholar 

  • Knyihar-Csillik, E., Csillik, B. &Rakic, P. (1982) 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 

  • Light, A. R. &Perl, E. R. (1979a) Reexamination of the dorsal root projection to the spinal dorsal horn including observations on the differential termination of coarse and fine fibers.Journal of Comparative Neurology 186, 117–32.

    Google Scholar 

  • Light, A. R. &Perl, E. R. (1979b) Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers.Journal of Comparative Neurology 186, 133–50.

    Google Scholar 

  • Lima, D. &Coimbra, A. (1986) A Golgi study of the neuronal population of the marginal zone (lamina I) of the rat spinal cord.Journal of Comparative Neurology 244, 53–71.

    Google Scholar 

  • Lima, D. &Coimbra, A. (1988) The spinothalamic system of the rat: structural types of retrogradely labelled neurons in the marginal zone (lamina I).Neuroscience 27, 215–30.

    Google Scholar 

  • Lima, D. &Coimbra, A. (1990) Structural types of marginal (lamina I) neurons projecting to the dorsal reticular nucleus of the medulla oblongata.Neuroscience 34, 591–606.

    Google Scholar 

  • Maxwell, D. J. &Rethelyi, M. (1987) Ultrastructure and synaptic connections of cutaneous afferent fibres in the spinal cord.Trends in Neuroscience 10, 117–23.

    Google Scholar 

  • McNeill, D. L., Coggeshall, R. E. &Carlton, S. M. (1988) A light and electron microscopic study of calcitonin gene-related peptide in the spinal cord of the rat.Experimental Neurology 99, 699–708.

    Google Scholar 

  • Merighi, A., Polak, J. M., Fumagalli, G. &Theodosis, D. T. (1989) Ultrastructual localization of neuropeptides and GABA in rat dorsal horn: a comparison of different immunogold labelling techniques.Journal of Histochemistry and Cytochemistry 37, 529–40.

    Google Scholar 

  • Molander, C. &Grant, G. (1985) Laminar distribution and somatotopic organization of primary afferent fibers from hindlimb nerves in the dorsal horn. A study by transganglionic transport of horseradish peroxidase in the rat.Neuroscience 9, 297–312.

    Google Scholar 

  • Molander, C., Xu, Q., Rivero-Melian, C. &Grant, G. (1989) Cytoarchitectonic organization of the spinal cord in the rat. II. The cervical and upper thoracic cord.Journal of Comparative Neurology 289, 375–85.

    Google Scholar 

  • Narotzky, R. A. &Kerr, F. W. L. (1978) Marginal neurons of the spinal cord: types, afferent synaptology and functional considerations.Brain Research 139, 1–20.

    Google Scholar 

  • Pickel, V. M., Reis, D. J. &Leeman, S. E. (1977) Ultrastructural localization of substance P in neurons of rat spinal cord.Brain Research 122, 534–40.

    Google Scholar 

  • Perl, E. R. (1984) Characterization of nociceptors and their activation of neurons in the superficial dorsal horn; first steps for the sensation of pain. InNeural Mechanisms of Pain (edited byKruger, L. &Liebeskind, J. C.) pp. 23–51. New York, Raven Press.

    Google Scholar 

  • Price, D. D., Hayashi, H., Dubner, R. &Ruda, M. A. (1979) Functional relationships between neurons of marginal and substantia gelatinosa layers of primate dorsal horn.Journal of Neurophysiology 42, 1590–1608.

    Google Scholar 

  • Ralston, H. J., III (1968) Dorsal root projections to dorsal horn neurons in the cat spinal cord.Journal of Comparative Neurology 132, 303–30.

    Google Scholar 

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

    Google Scholar 

  • Rexed, B. (1954) A cytoarchitectonic atlas of the spinal cord in the cat.Journal of Comparative Neurology 100, 297–379.

    Google Scholar 

  • Rethelyi, M., Light, A. R. &Perl, E. R. (1982) Synaptic complexes formed by functionally defined primary afferent units with fine myelinated fibers.Journal of Comparative Neurology 207, 381–93.

    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., Pignatelli, D. &Coimbra, A. (1985) Synaptic architecture of glomeruli in superficial dorsal horn, as shown in serial reconstructions.Journal of Neurocytology 238, 440–52.

    Google Scholar 

  • Ribeiro Da Silva, A., Tagari, P. &Cuello, C. (1989) Morphological characterization of substance P-like immunoreactive glomeruli in the superficial dorsal horn of the rat spinal cord and trigeminal subnucleus caudalis: a quantitative study.Journal Comparative of Neurology 281, 497–515.

    Google Scholar 

  • Ruda, M. A. &Gobel, S. (1980) Ultrastructural characterization of axonal endings in the substantia gelatinosa which take up (3H) serotonin.Brain Research 184, 57–83.

    Google Scholar 

  • Ruda, M. A., Allen, B. &Gobel, S. (1981) Ultrastructural analysis of medial stem afferents to the superficial dorsal horn.Brain Research 205, 175–80.

    Google Scholar 

  • Sugiura, Y., Lee, C. L. &Perl, E. R. (1986) Central projections of identified, unmyelinated (C) afferent fibers innervating mammalian skin.Science 234, 358–61.

    Google Scholar 

  • Sugiura, Y., Terui, N. &Hosoya, Y. (1989a) Difference in distribution of central terminal between visceral and somatic unmyelinated (C) primary afferent fibers.Journal of Neurophysiology 62, 834–40.

    Google Scholar 

  • Sugiura, Y., Terui, N., Hosoya, Y. &Kohno, K. (1989b) Distribution of unmyelinated primary afferent fibers in the dorsal horn. InProcessing of Sensory Information in the Superficial Dorsal Horn of the Spinal Cord (edited byCervero, F., Bennett, G. J. &Headley, P. M.) pp. 15–23. New York, London: Plenum Press.

    Google Scholar 

  • Willis, W. D. &Coggeshall, R. E. (1991) Structure of the dorsal horn. InSensory Mechanisms of the Spinal Cord (edited byWillis, W. D. &Coggeshall, R. E.). New York: Plenum Press.

    Google Scholar 

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Authors and Affiliations

  1. Institute of Histology and Embryology, Faculty of Medicine and Center of Experimental Morphology of the University of Oporto, 4200, Porto, Portugal

    F. Cruz, D. Lima & A. Coimbra

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  1. F. Cruz
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  2. D. Lima
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Cruz, F., Lima, D. & Coimbra, A. Periterminal synaptic organization of primary afferents in laminae I and IIo of the rat spinal cord, as shown after anterograde HRP labelling. J Neurocytol 22, 191–204 (1993). https://doi.org/10.1007/BF01246358

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  • DOI: https://doi.org/10.1007/BF01246358

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