Skip to main content
SpringerLink
Log in

Locus coeruleus terminals in intraocularly transplanted spinal cords as compared with catecholamine terminals in normal spinal cords: Their synaptic densities and functional considerations

  • Published:
Medical Electron Microscopy Aims and scope Submit manuscript

Abstract

Locus coeruleus terminals in intraocularly transplanted spinal cords and catecholamine terminals in defined areas of normal spinal cords were investigated qualitatively and quantitatively by immunoelectron microscopy. Results showed that the morphological features of synapses formed in the grafts closely resembled those of normal spinal cords. The incidences of synapses per varicosities, as observed in single sections, were 30.1, 40.2 and 22.8% for the ventral horn, dorsal horn and grafted spinal cord, respectively. In all three groups, most of the postsynaptic targets were small dendrites, although high frequencies of large dendrites were found in the ventral horn. Spines and axons in the grafts were also postsynaptic targets. Several characteristics of relative immaturity were observed in the grafts. It is suggested that the inhibition of spinal neurons by locus coeruleus terminals may be mediated not only by volume transmission through nonsynaptic contacts, but also by direct contacts with catecholamine terminals, and that the excitation of facilitation observed at those terminals may be explained by the suppression of inhibitory neurons by axoaxonic contacts.

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

  1. Raisman, G. andField, P.M. A quantitative investigation of the development of collateral reinnervation after partial deafferentation of the septal nuclei.Brain Res. 50, 241–264 (1973).

    Article  CAS  PubMed  Google Scholar 

  2. McWilliams, R., andLynch, G.: Terminal proliferation and synaptogenesis following partial deafferentiation: the reinnervation of the inner molecular layer of the dentate gyrus following removal of its commissural afferents.J. Comp. Neurol. 180, 581–616 (1978).

    Article  CAS  PubMed  Google Scholar 

  3. Cotman, C.W., andNadler, J.V.: Reactive synaptogenesis in the hippocampus.In: Neuronal Plasticity (Cotman, C.W. ed.), p. 227–271, Raven Press, New York, 1978.

    Google Scholar 

  4. Murray, M.: Reactive synaptogenesis in the CNS. A comparison of regenerating and sprouting systems.Neurochem. Pathol. 5, 205–220 (1986).

    CAS  PubMed  Google Scholar 

  5. Steward, O.: Regulation of synaptogenesis through the local synthesis of protein at the postsynaptic site.Prog. Brain Res. 71, 267–279 (1987).

    CAS  PubMed  Google Scholar 

  6. Freund, T.F., Bolam, J.P., Björklund, A., Stenevi, U., Dunnett, S.B., Powell, J.F., andSmith, A.D. Efferent synaptic connections of grafted dopaminergic neurons reinnervating the host neostriatum: a tyrosin hydroxylase immunocytochemical study.J. Neurosci. 5, 603–616 (1985).

    CAS  PubMed  Google Scholar 

  7. Mahalik, T.J., Finger, T.E., Strömberg, I., andOlson, L.: Substantia nigra transplants into denervated striatium of the rat: ultrastructure of graft and host interconnections.J. Comp. Neurol. 240, 60–70 (1985).

    Article  CAS  PubMed  Google Scholar 

  8. Clarke, D.J., Gage, F.H., Dunnett, S.B., Nilsson, O.G., andBjörklund, A.: Symptogenesis of grafted cholinergic neurons.Ann. N.Y. Acad. Sci. 445, 268–283 (1987).

    Google Scholar 

  9. Sørensen, T., Finsen, B., andZimmer, J.: Nerve connections between mouse and rat hippocampal brain tissue: ultrastructural observations after intracerebral xenografting.Brain Res. 413, 392–397 (1987).

    Article  PubMed  Google Scholar 

  10. Satoh, K., Tohyama, M., Yamamoto, K., andShimizu, N.: Noradrenaline innervation of the spinal cord studied by the horseradish peroxidase method combined with monoamine oxidase staining.Exp. Brain Res. 30, 175–186 (1977).

    Article  CAS  PubMed  Google Scholar 

  11. Nygren, L.-G., andOlson, L.: A new major projection from locus coeruleus: the main source of noradrenergic nerve terminals in the ventral and dorsal columns of the spinal cord.Brain Res. 132, 85–93 (1977).

    Article  CAS  PubMed  Google Scholar 

  12. Commissiong, J.W., Hellström, S.O., andNeff, N.H.: A new projection from locus coeruleus to the spinal ventral columns: histochemical and biochemical evidence.Brain Res. 148, 207–213 (1978).

    Article  CAS  PubMed  Google Scholar 

  13. Fleetwood-Walker, S.M., andCoote, J.H.: The contribution of brain stem catecholamine cell groups to the innervation of the sympathetic lateral cell column.Brain Res. 205, 141–155 (1981).

    Article  CAS  PubMed  Google Scholar 

  14. Westlund, K.N., Bowker, R.M., Ziegler, M.G., andCoulter, J.D.: Noradrenergic projections to the spinal cord of the rat.Brain Res. 263 15–31 (1983).

    Article  CAS  PubMed  Google Scholar 

  15. Cabana, T., andMartin, G.F.: Developmental sequence in the origin of descending spinal pathways. Studies using retrograde transport techniques in the North American opossum (Didelphis Virginiana).Dev. Brain Res. 15, 247–263 (1984).

    Article  Google Scholar 

  16. Chen, K.S., andStanfield, B.B.: Evidence that selective collateral elimination during postnatal development results in a restriction in the distribution of locus coeruleus neurons which project to the spinal cord in rats.Brain Res. 410, 154–158 (1987).

    CAS  PubMed  Google Scholar 

  17. Descarries, L., Watkins, K.C., andLapierre, Y.: Nuradrenergic axon terminals in the cerebral cortex of rat. Topometric ultrastructural analysis.Brain Res. 133, 197–222 (1977).

    Article  CAS  PubMed  Google Scholar 

  18. Koda, L.Y., andBloom, F.E.: A light and electron microscopic study of noradrenergic terminals in the rat dentate gyrus.Brain Res. 120, 327–335 (1977).

    Article  CAS  PubMed  Google Scholar 

  19. Olschowka, J.A., Molliver, M.E., Grzanna, R., Rice, F.L., andCoyle, J.T.: Ultrastructural demonstration of noradrenergic synapses in the rat central nervous system by dopamine-B-hydroxylase immunocytochemistry.J. Histochem. Cytochem. 29, 271–280 (1981).

    CAS  PubMed  Google Scholar 

  20. Beaudet, A., andDescarries, L.: Fine structure of monoamine axon terminals in cerebral cortex.In: Monoamine Innervation of Cerebral Cortex (Descarries, L., Reader, T.H. andJasper, H.H. ed.), p. 77–93, Alan R. Liss, New York, 1984.

    Google Scholar 

  21. Séguéla, P., Watkins, K.C., Geffard, M., andDescarries, L.: Noradrenaline axon terminals in adult rat neocortex: an immunocytochemical analysis in serial thin sections.Neuroscience,35, 249–264 (1990).

    PubMed  Google Scholar 

  22. Rajaofetra, N., Ridet, J.-L., Poulat, P., Marlier, L., Sandillon, F., Geffard, M., andPrivat, A.: Immunocytochemical mapping of noradrenergic projections to the rat spinal cord with an antiserum against noradrenaline.J. Neurocytol. 21, 481–494 (1992).

    Article  CAS  PubMed  Google Scholar 

  23. Ridet, J.-L., Rajaofetra, N., Teilhac, J.-R., Geffard, M. andPrivat, A.: Evidence for nonsynaptic serotonergic and noradrenergic innervation of the rat dorsal horn and possible involvement of neuron-glia interactionsNeuroscience,52, 143–157 (1993).

    Article  CAS  PubMed  Google Scholar 

  24. Foote, S.L., Bloom, F.E., andAston-Jones, G.: Nucleus locus coeruleus: new evidence of anatomical and physiological specificity.Physiol. Rev. 63, 844–914 (1983).

    CAS  PubMed  Google Scholar 

  25. Kojima, M., Matsuura, T., Tanaka, A., Amagai, T., Imanishi, J. andSano, Y.: Characteristic distribution of noradrenergic terminals on the anterior horn motoneurons innervating the perineal striated muscles in the rat.Anat. Embryol. 171, 267–273 (1985).

    Article  CAS  PubMed  Google Scholar 

  26. Papadopoulos, G.C., Parnavelas, J.G.. andBuijis, R.: Monoaniergic fibers form conventional synapses in the cerebral cortex.Neurosci. Lett. 76, 275–279 (1987).

    Article  CAS  PubMed  Google Scholar 

  27. Silverman, W.F., Aravich, P.F., Collier, T.J., Olshowka, J.A. andSladek Jr., J.R.: Reinhervation of transplanted hypothalamic neurons by host aminegic fibers in rats.Brain Res. 412, 375–380 (1987).

    Article  CAS  PubMed  Google Scholar 

  28. Inoue, H.K., Henschen, A.. andOlson, L.: Ultrastructure of spinal cord grafts with and without cografts coeruleus in oculo.Exp. Neurol. 102, 109–120 (1988).

    Article  CAS  PubMed  Google Scholar 

  29. Hagihira, S., Senba, E., Yoshida, S., Tohyama, M.. andYoshida, I.: Fine structure of noradrenergic terminals and their synapses in the rat spinal dorsal horn: an immunohistochemical study.Brain Res. 526, 73–80 (1990).

    Article  CAS  PubMed  Google Scholar 

  30. Doyle, C.A.. andMaxwell, D.J.: Catecholaminergic innervation of the spinal dorsal horn: a correlated light and electron microscopic analysis of tyrosine hydroxylase-immunoreactive fibers in the cat.neuroscience,45, 161–176 (1991).

    Article  CAS  PubMed  Google Scholar 

  31. Marshall, K.C.: Catecholamines and their actions in the spinal cord.In: Handbook of the Spinal Cord: Pharmacology, Vol. 1 (Davidoff, J.A. ed.), p. 275–328. Marcell Decker, New York, 1983.

    Google Scholar 

  32. Ossipov, M.H., Catterjee, T.K.. andGebhart, G.F.: Locus coeruleus lesions in the rat enhance the antinociceptive potency of centrally administered clonidine but nomorphine.Brain Res. 341, 320–330 (1985).

    Article  CAS  PubMed  Google Scholar 

  33. Jones, S.L.. andGebhart, G.F.: Characterization of coeruleospinal inhibition of the nociceptive tail-flick reflick reflex in the rat: mediation by spinal adrenocepters.Brain Res. 364, 315–330 (1986).

    Article  CAS  PubMed  Google Scholar 

  34. Janss, A.J., Jones, S.L.. andGebhart, G.F.: Effect of spinal norepinephrine depletion on descending inhibition of the tail flick reflex from the locus coeruleus and lateral reticular nucleus in the rat.Brain Res. 400, 40–52 (1987).

    Article  CAS  PubMed  Google Scholar 

  35. Chan, J.Y.H., Fung, S.J., Chan, S.H.H.. andBarnes, C.D.: Facititation of lumbar monosynaptic reflexes by locus coeruleus in the rat.Brain Res. 369, 103–109 (1986).

    Article  CAS  PubMed  Google Scholar 

  36. Hino, M., Ono, H.. andFukuda, H.: Involvement of noradrenergic systems in the effects of conditioning stimulation the lower brain stem on the lumbar spinal reflex in rats.Gen. Pharmacol. 18, 41–45 (1987).

    CAS  PubMed  Google Scholar 

  37. Fung, S.J., Pompeiano, O.. andBarnes, C.D.: Seppression of the recurrent inhibitory pathway in lumbar cord segments during locus coeruleus stimualtion in cats.,Brain Res. 402, 351–354 (1987).

    CAS  PubMed  Google Scholar 

  38. Henschen, A., Goldstein, M.. andOlson, L.: The innervation of intraocular spinal cord transplants by cografts of locus coeruleus and substantia nigra neurons.Rev. Brain Res. 36, 237–247 (1987).

    Google Scholar 

  39. Olson, L., Seiger, Å.. andStrömberg, I.: Intraocular transplantation in rodents. A detailed account of the procedure and examples of its use in neurobiology with special reference to brain tissue grafting.In: Advances in Cellular Neurobiology, Vol. 4 (Fedoroff, S. andHertz, L. ed.), p. 407–442, Academic Press, New York, 1983.

    Google Scholar 

  40. Seiger, Å.. andOlson, L.: Quantification of fiber growth in transplanted central monoamine neurons,Cell. Tissue Res.,17, 285–316 (1977).

    Google Scholar 

  41. Nagatsu, I., Kondo, Y., Inagaki, S., Karasawa, H., Kato, T. andNagatsu, T.: Immunofluorescent studies on tyrosine hydroxylase: application for its axoplasmic transport.Acta Histochem. Cytochem. 10, 494–499 (1977).

    CAS  Google Scholar 

  42. Freund, T.F., Powell, J.F.. andSmith, A.D.: Tyrosine hydroxylase immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines.Neuroscience,13, 1189–1215 (1984).

    Article  CAS  PubMed  Google Scholar 

  43. Shirao, T., Inoue, H.K., Kano, Y.. andObata, K.: Localization of a developmentally regulated neuron-specific protein S54 in dendrites as revealed by immunoelectron microscopy.Brain Res. 413, 374–378 (1987).

    Article  CAS  PubMed  Google Scholar 

  44. Zivin, J.A., Reid, J.L., Tappaz, M.L.. andKopin, I.J.: Quantitative localization of tyrosine hydroxylase, and glutamic acid decarboxylase in spinal cord.Brain Res. 105, 151–156 (1976).

    Article  CAS  PubMed  Google Scholar 

  45. Love, S.: An experimental study of peripheral nerve regeneration after X-irradiation.Brain Res. 106, 39–54 (1983).

    Google Scholar 

  46. Longo, F.M., Hayman, E.G., Davis, G.E., Rouslahti, E., Engvall, E., Manthorpe, M.. andVaron, S.: Neuritepromoting factors and extracellular matrix components accumulatingin vivo within nerve regeneration chamber.Brain Res. 309, 105–117 (1984).

    Article  CAS  PubMed  Google Scholar 

  47. Bunge, M.B., Johnson, M.I., Ard, M.D.. andKleitman, N.: Factors influencing the growth of regenerating nerve fibers in culture.Prog. Brain Res. 71, 61–67 (1987).

    CAS  PubMed  Google Scholar 

  48. Inoue, H.K.. andOlson, L.: Ultrastructural investigation of nerve regenerationin vivo—Comparison within vitro neurite formation.Neurol. Med.-Chir. 29, 799–805 (1989).

    CAS  Google Scholar 

  49. Marlier, L., Sandillon, F., Poulat, P., Rajaofetra, N., Geffard, M.. andPrivat, A.: Seretonergic innervation of the dorsal horn of rat spinal cord: light and electron microscopic immunocytochemical study.J. Neurocytol. 20, 310–322 (1991).

    Article  CAS  PubMed  Google Scholar 

  50. Clark, F.M., Yeomans, D.C.. andProudfit, H.K.: The noradrenergic innervation of the spinal cord: differences between two substrains of Sprague-Dawley rats determined using retrograde tracers combined with immunocytochemistry.Neurosci. Lett. 125, 155–158 (1991).

    Article  CAS  PubMed  Google Scholar 

  51. Campbell, G.. andFrost, D.O.: Target-controlled differentiation of axon terminals and synaptic organization.Proc. Natl. Acad. Sci. USA,84, 6929–6933 (1987).

    CAS  PubMed  Google Scholar 

  52. Specht, L.A., Pickel, V.M., Joh, T.H.. andReis, D.J.: Fine structure of the nigrostriatel anlarge in fetal rat brain by immunocytochemical localization of tyrosine hydroxylase.Brain Res. 218, 49–65 (1981).

    Article  CAS  PubMed  Google Scholar 

  53. Henden, A., Goldstein, M.. andPalmer, M.R.: Evidence for functional contacts between cografted locus coeruleus and spinal cord in oculo: electrophysiological studies.Brain Res. 474, 66–74 (1988).

    Google Scholar 

  54. Ruda, M.A., Coffield, J.. andSteinbusch, H.W.: Immunocytochemical analysis of serotonergic axons in laminae 1 and 2 of the lumber spinal cord of the cat.J. Neurosci. 2, 1660–1671 (1981).

    Google Scholar 

  55. De Lanerolle, N.C.. andLa Motte, C.C.: Ultrastructure of chemically defined neuron systems in the dorsal horn of the monkey. I. Substance P immunoreactivity.Brain Res. 274, 31–49 (1983).

    PubMed  Google Scholar 

  56. La Motte, C.C.. andDe Lanerolle, N.C.: Ultrastructure of chemically defined neuron systems in the dorsal horn of the monkey. II. Methionine-enkephalin immunoreactivity.Brain Res. 274, 51–63 (1983).

    Google Scholar 

  57. Ulfhake, B., Arvidsson, U., Cullheim, S., Hökfelt, T., Brodin, E., Verhofstad, A.. andVisser, T.: An ultrastructural study of 5-hydroxytryptamine-, thyrotropin-releasing hormone- and substance P-immunoreactive axonal boutons in the motor nucleus of spinal cord segments L7-S1 in the adult cat.Neuroscience,23, 917–929 (1987).

    Article  CAS  PubMed  Google Scholar 

  58. Réthelyi, M., Light, A.R.. andPerl, E.R.: Synaptic complexes formed by functionally defined primary afferent units with fine myelinated fibers.J. Comp. Neurol. 207, 381–393 (1982).

    PubMed  Google Scholar 

  59. Magoul, R., Onteniente, B., Gaffard, M.. andCalas, A.: Anatomical distribution and ultrastructural organization of the GABAergic system in the rat spinal cord. An immunocytochemical study using anti-GABA antibodies.Neuroscience,20, 1001–1009 (1987).

    Article  CAS  PubMed  Google Scholar 

  60. McLaughlin, B.J., Barber, R., Saito, K., Roberts, E. andWu, J.-Y.: Immunohistochemical localization of glutamate decarboxylase in rat spinal cord.J. Comp. Neurol. 168, 303–312 (1975).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neuroscience, Karolinska Institute, S-104 01, Stockholm 60, Sweden

    Hiroshi K. Inoue, Andreas Henschen & Lars Olson

  2. Department of Neurosurgery, Gunma University School of Medicine, 3-39, Showa-machi, 371, Maebashi, Japan

    Hiroshi K. Inoue

  3. Department of Anatomy, Fujita-Gukuen Health University, 1-98, Dengakugakubo, Kutsukake, 470-11, Toyoake, Japan

    Ikuko Nagatsu

Authors
  1. Hiroshi K. Inoue
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andreas Henschen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ikuko Nagatsu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lars Olson
    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

Inoue, H.K., Henschen, A., Nagatsu, I. et al. Locus coeruleus terminals in intraocularly transplanted spinal cords as compared with catecholamine terminals in normal spinal cords: Their synaptic densities and functional considerations. Med Electron Microsc 27, 123–135 (1994). https://doi.org/10.1007/BF02348177

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02348177

Key words

Search

Navigation