Skip to main content
SpringerLink
Log in

Morphology and distribution of primary afferent fibres expressing α-galactose extended oligosaccharides in the spinal cord and brainstem of the rat. Light microscopy

  • Published:
Journal of Neurocytology

Summary

The light microscopic morphology and distribution of non-substance P-containing small primary afferent fibres were studied. These fibres were labelled using LD2 and LA4 monoclonal antibodies which recognize α-galactose extended oligosaccharides expressed by primary afferent neurons. The LD2 and LA4 antibodies immunostained small primary afferent fibres ending mainly in lamina II of the spinal cord dorsal horn and trigeminal subnucleus caudalis of the rat. The lamination pattern of both types of primary afferents was assessed using an image analysis system. The highest density of LD2-immunoreactive fibres was located in a patchy band located in lamina II outer, while LA4-immunoreactive fibres were distributed mainly through lamina II inner. In lateral regions of cervical and lumbar dorsal horn the LA4-immunoreactive band is broader and comprises almost all lamina II. In contrast to substance P-containing primary afferents, a low density of LD2- or LA4-immunoreactive fibres was found in lamina I, and no terminal fields were found in lamina V or lamina X of the spinal cord or in levels of the trigeminal system outside the subnucleus caudalis. Both antibodies also labelled the parent fibres in the white matter fascicles. LD2-immunoreactive fibres were located in the dorsal roots, medial regions of the Lissauer tract, dorsal columns of the spinal cord, outer regions of the spinal trigeminal tract and dorsal to the cuneatus and gracilis nuclei. In contrast, LA4-immunoreactive fibres were restricted to the dorsal roots, medial and lateral regions of the Lissauer tract and the outer regions of the trigeminal tract. Immunostained fibres in the rootlets of the X and IX nerves and immunoreactive terminal arborizations in various subnuclei of the nucleus tractus solitarius were seen using both antibodies. These results show that subpopulations of small primary afferents stained by LD2 and LA4 antibodies have distinct patterns of central distribution and are consistent with a subdivision of small primary afferents into peptide- and non-peptide-containing groups.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alvarez, F. J. &Priestley, J. V. (1989) Circuitry of somatostatin-containing elements in laminae I and II of the rat trigeminal nucleus.Abstracts 12th European Neuroscience Association.

  • Alvarez, F. J., Rodrigo, J., Jessell, T. M., Dodd, J. &Priestley, J. V. (1989) Ultrastructure of primary afferent fibres and terminals expressing α-galactose extended oligosaccharides in the spinal cord and brainstem of the rat.Journal of Neurocytology 18, 631–45.

    Google Scholar 

  • Barber, R. P., Vaughn, J. E., Randall, G., Slemmon, J., Salvaterra, P. M., Roberts, E. &Leeman, S. E. (1979) The origin, distribution and synaptic relationships of substance P axons in rat spinal cord.Journal of Comparative Neurology 184, 331–52.

    Google Scholar 

  • Bowker, R. M. &Abbott, L. C. (1988) The origins and trajectories of somatostatin reticulospinal neurons: a potential neurotransmitter candidate of the dorsal reticulo spinal pathway.Brain Research 447, 398–404.

    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 

  • Chou, D. K. H., Dodd, J., Jessell, T. M., Costello, C. E., &Jungalwala, F. B. (1989) Identification of α-galactose (α-fucose)-asialo-GM1 glycolipid expressed by subsets of rat dorsal root ganglion neurons.Journal of Biological Chemistry 264, 3409–15.

    Google Scholar 

  • Chung, K. &Coggeshall, R. E. (1985) Unmyelinated primary afferent fibres in dorsal funiculi of cat sacral spinal cord.Journal of Comparative Neurology 238, 365–9.

    Google Scholar 

  • Chung, K., Langford, L. A. &Coggeshall, R. E. (1987) Primary afferent and propiospinal fibres in the rat dorsal and dorsolateral funiculi.Journal of Comparative Neurology 263, 68–75.

    Google Scholar 

  • Chung, K., Lee, W. T. &Carlton, S. M. (1988) The effects of dorsal rhizotomy and spinal cord isolation on calcitonin gene-related peptide containing terminals in the cat lumbar dorsal horn.Neuroscience Letters 90, 27–32.

    Google Scholar 

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

  • Colin, S. &Kruger, L. (1986) Peptidergic nociceptive axon visualization in whole-mount preparations of cornea and tympanic membrane in rat.Brain Research 398, 199–203.

    Google Scholar 

  • Cuello, A. C., Del Fiacco, M. &Paxinos, G. (1978) The central and peripheral ends of the substance P-containing primary sensory neurons in the rat trigeminal system.Brain Research 152, 499–510.

    Google Scholar 

  • Dalsgaard, C. J., Hökfelt, T., Johansson, O. &Elde, R. (1981) Somatostatin immunoreactive cell bodies in the dorsal horn and the parasympathetic intermediolateral nucleus of the rat spinal cord.Neuroscience Letters 27, 335–40.

    Google Scholar 

  • Del Fiacco, M. &Cuello, A. C. (1980) Substance P- and enkephalin-containing neurons in the rat trigeminal system.Neuroscience 7, 1127–39.

    Google Scholar 

  • Dodd, J. &Jessell, T. M. (1985) Lactoseries carbohydrates specify subsets of dorsal root ganglion neurons projecting to the superficial dorsal horn of rat spinal cord.journal of Neuroscience 5, 3278–94.

    Google Scholar 

  • Dodd, J. &Jessele, T. M. (1986) Cell surface glycoconjugates and carbohydrate-binding proteins: possible recognition signals in sensory neurone development.Journal of Experimental Biology 124, 225–38.

    Google Scholar 

  • Dodd, J., Solter, D. &Jessell, T. M. (1984) Monoclonal antibodies against carbohydrate differentiation antigens identify subsets of primary sensory neurons.Nature 311, 469–72.

    Google Scholar 

  • Dubner, R. &Bennett, G. J. (1983) Spinal and trigeminal mechanisms of nociception.Annual Review of Neuroscience 6, 381–418.

    Google Scholar 

  • Fischer, J. &Csillik, B. (1985) Lectin binding: a genuine marker for transganglionic regulation of human primary sensory neurons.Neuroscience Letters 54, 132–45.

    Google Scholar 

  • Gibson, S. J., Polar, J. M., Bloom, S. R., Sabate, I. M., Mulderry, P. K., Ghatei, M. A., Morrison, J. F. B., Kelly, J. S., Rosenfeld, M. G. &Evans, R. (1984) Calcitonin gene-related peptide (CGRP)-immunoreactivity in the spinal cord of man and eight other species.Journal of Neuroscience 4, 3101–11.

    Google Scholar 

  • Gobel, S. &Purvis, M. B. (1972) Anatomical studies of the organization of the spinal V nucleus: the deep bundles and the spinal V tract.Brain Research 48, 27–44.

    Google Scholar 

  • Görcs, T. J., Léránth, C. &MacLusky, N. J. (1986) The use of gold-substituted silver-intensified diaminobenzidine (DAB) and non-intensified DAB for simultaneous electron microscopic immunoperoxidase labelling of tyrosine hydroxylase and glutamic acid decarboxylase immunoreactivity in the rat medial proptic area.Journal of Histochemistry and Cytochemistry 54, 1439–47.

    Google Scholar 

  • Harper, A. A. &Lawson, S. N. (1985) Conduction velocity is related to morphological cell type in rat dorsal root ganglion neurons,Journal of Physiology 359, 31–46.

    Google Scholar 

  • Hökfelt, T., Johansson, O., Luft, R. &Arimura, A. (1975a) Immunohistochemical evidence for the presence of somatostatin, a powerful inhibitory peptide, in some primary sensory neurons.Neuroscience Letters 1, 231–5.

    Google Scholar 

  • Hökfelt, T., Johansson, O., Luft, R., Nilsson, G. &Arimura, A. (1976) Immunohistochemical evidence for separate populations of somatostatin-containing and substance P-containing primary afferent neurons in rat.Neuroscience 1, 131–6.

    Google Scholar 

  • Hökfelt, T., Kellerth, J. O., Nilsson, G. &Pernow, B. (1975b) Experimental immunohistochemical studies on the localization and distribution of substance P in cat primary sensory neurons.Brain Research 100, 235–52.

    Google Scholar 

  • Hunt, S. P., Kelly, J. S., Emson, P. C., Kimmell, J., Miller, R. &Wu, J. Y. (1981) An immunohistochemical study of neuronal subpopulations containing neuropeptides or GABA within the superficial layers of the rat dorsal horn.Neuroscience 5, 1871–90.

    Google Scholar 

  • Hunt, S. P. &Rossi, J. (1985) Peptide- and non-peptide-containing unmyelinated primary afferents: the parallel processing of nociceptive information.Philosophical Transactions of the Royal Society of London, Series B 308, 283–9.

    Google Scholar 

  • Jacquin, M. F., Semba, K., Rhoades, R. W. &Egger, M. D. (1982) Trigeminal primary afferents project bilaterally to dorsal horn and ipsilaterally to cerebellum, reticular formation, and cuneate, solitary, supratrigeminal and vagal nuclei.Brain Research 246, 285–91.

    Google Scholar 

  • Jancsóp, G. &Király, E. (1980) Distribution of chemosensitive primary sensory afferents in the central nervous system of the rat.Journal of Comparative Neurology 190, 781–92.

    Google Scholar 

  • Jessell, T. M. &Dodd, J. (1985) Structure and expression of differentiation antigens on functional subclasses of primary sensory neurons.Philosophical Transactions of the Royal Society of London, Series B 308, 271–81.

    Google Scholar 

  • Jessell, T. M. &Dodd, J. (1986) Neurotransmitters and differentiation antigens in subsets of sensory neurons projecting to the spinal dorsal horn. InNeuropeptides in Neurologic and Psychiatric Disease (edited byMartin, J. B. &Barchas, J. D.), pp. 111–33. New York: Raven Press.

    Google Scholar 

  • Ju, G., Hökfelt, T., Brodin, E., Fahrenkrug, J., Fischer, J. A., Frey, P., Elde, R. P. &Brown, J. C. (1987) Primary sensory neurons of the rat showing calcitonin gene-related peptide immunoreactivity and their relation to substance P-, galanin-, vasoactive intestinal polypeptide- and cholecystokinin-immunoreactive ganglion cells.Cell and Tissue Research 247, 417–31.

    Google Scholar 

  • Kalia, M. &Sullivan, J. M. (1982) Brainstem projections of sensory and motor components of the vagus nerve in the rat.Journal of Comparative Neurology 211, 248–64.

    Google Scholar 

  • Kawai, Y., Takami, K., Shiosaka, S., Emson, P. C., Hillyard, C. J., Girgis, S., MacIntyre, I. &Tohyama, M. (1985) Topographic localization of calcitonin gene-related peptide in the rat brain: an immunohistochemical study.Neuroscience 15, 747–64.

    Google Scholar 

  • Kruger, L., Sternini, C., Brecha, N. C. &Mantyh, P. W. (1988) Distribution of calcitonin gene-related peptide immunoreactivity in relation to the rat central somatosensory projection.Journal of Comparative Neurology 273, 149–62.

    Google Scholar 

  • Lawson, S. N., Harper, A. A., Harper, E. I., Garson, J. A. &Anderton, B. H. (1984) A monoclonal antibody against neurofilament protein specifically labels a sub-population of rat sensory neurons.Journal of Comparative Neurology 228, 263–72.

    Google Scholar 

  • Lawson, S. N., Harper, E. I., Harper, A. A., Garson, J. A., Coakham, H. B. &Randall, B. J. (1985) Monoclonal antibody 2C5, a marker for a subpopulation of small neurons in rat DRG.Neuroscience 16, 365–74.

    Google Scholar 

  • Ljungdahl, A., Hökfelt, T. &Nilsson, G. (1978) Distribution of substance P-like immunoreactivity in the central nervous system of the rat-I. Cell bodies and nerve terminals.Neuroscience 3, 861–943.

    Google Scholar 

  • Marfurt, C. F. &Del Toro, D. R. (1987) Corneal sensory pathway in the rat: a horseradish peroxidase tracing study.Journal of Comparative Neurology 261, 450–9.

    Google Scholar 

  • Marfurt, C. F. &Turner, D. F. (1984) The central projection of tooth pulp afferent neurons in the rat as determined by the transganglionic transport of horseradish peroxidase.Journal of Comparative Neurology 223, 535–47.

    Google Scholar 

  • McNeill, D. L., Chung, K., Carlton, S. M. &Coggeshall, R. E. (1988a) Calcitonin gene-related peptide immunostained axons provide evidence for fine primary afferent fibres in the dorsal and dorsolateral funiculi of the rat spinal cord.Journal of Comparative Neurology 272, 303–8.

    Google Scholar 

  • McNeill, D. L., Coggeshall, R. E. &Carlton, S. M. (1988b) 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 

  • Millhorn, D. E., Seroogy, K., Hökfelt, T., Schemd, L. C., Terenius, L., Bucham, A. &Brown, J. C. (1987) Neurons of the ventral medulla oblongata that contain both somatostatin and enkephalin immunoreactivities project to nucleus tractus solitarius and spinal cord.Brain Research 424, 99–108.

    Google Scholar 

  • Nagy, J. T. &Hunt, S. P. (1982) Fluoride resistant acid phosphatase-containing neurons in dorsal root ganglia are separate from those containing substance P or somatostatin.Neuroscience 7, 89–97.

    Google Scholar 

  • Nashold, B. S. &Friedman, H. (1972) Dorsal column stimulation for control of pain. Preliminary report on 30 patients.Journal of Neurosurgery 36, 590–7.

    Google Scholar 

  • Paxinos, G. &Watson, C. (1982) The rat brain in stereotaxic coordinates. Sydney: Academic Press.

    Google Scholar 

  • Priestley, J. V., Somogyi, P. &Cuello, A. C. (1982) Immunocytochemical localization of substance P in the spinal trigeminal nucleus of the rat: a light and electron microscopic study.Journal of Comparative Neurology 221, 31–49.

    Google Scholar 

  • Regan, L., Dodd, J., Barondes, S. H. &Jessell, T. M. (1986) Selective expression of endogenous lactose-binding lectins and lactoseries glycoconjugates in subsets of rat sensory neurons.Proceedings of the National Academy of Sciences USA 83, 2248–52.

    Google Scholar 

  • Ribeiro-Da-Silva, A., Castro-Lopes, J. M. &Coimbra, A. (1986) Distribution of glomeruli with fluoride-resistant acid phosphatase (FRAP)-containing terminals in the substantia gelatinosa of the rat.Brain Research 377, 323–9.

    Google Scholar 

  • Ritter, S. &Dinh, T. T. (1988) Capsaicin-induced neuronal degeneration: Silver impregnation of cell bodies, axons and terminals in the central nervous system of the rat.Journal of Comparative Neurology 271, 79–90.

    Google Scholar 

  • Robertson, B. &Grant, G. (1989) Immunocytochemical evidence for the localization of the GM1 ganglioside in carbonic anhydrase-containing and RT97-immunoreactive rat primary sensory neurons.Journal of Neurocytology 18, 77–86.

    Google Scholar 

  • Schroeder, H. D. (1984) Somatostatin in the caudal spinal cord. An immunohistochemical study of the spinal centers involved in the innervation of pelvic organs.Journal of Comparative Neurology 223, 400–14.

    Google Scholar 

  • Silverman, J. D. &Kruger, L. (1988a) Acid phosphatase as a selective marker for a class of small sensory ganglion cells in several mammals: spinal cord distribution, histochemical properties and relation to fluoride-resistant acid phosphatase (FRAP) of rodents.Somatosensory Research 5, 219–46.

    Google Scholar 

  • Silverman, J. D. &Kruger, L. (1988b) Lectin and neuropeptide labelling of separate populations of dorsal root ganglion neurons and associated ‘nociceptor’ thin axons in rat testis and cornea whole-mount preparations.Somatosensory Research 5, 259–67.

    Google Scholar 

  • Skofitsch, G. &Jacobowitz, D. M. (1985) Calcitonin gene-related peptide: detailed immunohistochemical distribution in the central nervous system.Peptides 6, 721–15.

    Google Scholar 

  • Stine, S. M., Yang, H. Y. &Costa, E. (1982) Evidence for ascending and descending intraspinal as well as primary sensory somatostatin projections in the rat spinal cord.Journal of Neurochemistry 38, 1144–50.

    Google Scholar 

  • Streit, W. J. &Kreutzberg, G. W. (1987) Lectin binding by resting and reactive microglia.Journal of Neurocytology 16, 249–60.

    Google Scholar 

  • Streit, W. J., Schulte, B. A., Balentine, J. D. &Spicer, S. S. (1985) Histochemical localization of galactose-containing glycoconjugates in sensory neurons and their processes in the central and peripheral nervous system of the rat.Journal of Histochemistry and Cytochemistry 33, 1042–52.

    Google Scholar 

  • Streit, W. J., Schulte, B. A., Balentine, J. D. &Spicer, S. S. (1986) Evidence for glyconjugate in nociceptive primary sensory neurons and its origin from the Golgi complex.Brain Research 377, 1–17.

    Google Scholar 

  • Traub, R. J. &Mendell, L. M. (1988) The spinal projection of individual identified Aδ and C fibres.Journal of Neurophysiology 59, 41–55.

    Google Scholar 

  • Wakisaka, S., Ichikawa, H., Nishikawa, S., Matsuo, S., Takano, Y. &Akai, M. (1987) The distribution and origin of calcitonin-gene-related peptide-containing nerve fibres in feline dental pulp. Relationship with SP-containing nerve fibres.Histochemistry 86, 585–9.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departments of Physiology and Biochemistry, UMDS St Thomas's Campus, Lambeth Palace Road, SEI 7EH, London, UK

    F. J. Alvarez & J. V. Priestley

  2. Department of Neuroanatomy, Cajal Institute, Velazquez 144, 28007, Madrid, Spain

    J. Rodrigo

  3. Center for Neurobiology and Behavior, Columbia University, College of Physicians and Surgeons, 10032, New York, NY, USA

    T. M. Jessell & J. Dodd

  4. Howard Hughes Medical Institute, Columbia University, College of Physicians and Surgeons, 10032, New York, NY, USA

    T. M. Jessell

Authors
  1. F. J. Alvarez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Rodrigo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. M. Jessell
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Dodd
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. V. Priestley
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alvarez, F.J., Rodrigo, J., Jessell, T.M. et al. Morphology and distribution of primary afferent fibres expressing α-galactose extended oligosaccharides in the spinal cord and brainstem of the rat. Light microscopy. J Neurocytol 18, 611–629 (1989). https://doi.org/10.1007/BF01187082

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01187082

Keywords

Search

Navigation