Skip to main content
SpringerLink
Log in

Localization of substance P-like immunoreactivity in neurons and nerve terminals in the neostriatum of the rat: a correlated light and electron microscopic study

  • Published:
Journal of Neurocytology

Summary

An antiserum, to substance P has been used to study the neostriatum of rats which has received intracerebral injections of colchicine. Both cell bodies and nerve fibres were found to display immunoreactivity. Some of the fibres were swollen and could be traced back to their parent: cell body.

Examination in the electron microscope of structures that had first been identified in the light microscope showed that there are two different types of substance P-immunoreactive cell body. The first kind (type I) of immunoreactive cell body was of medium size and had a smooth surfaced nucleus. It displayed the ultrastructural features typical of medium-size spiny neurons. Identified axons of type I neurons gave rise to immunoreactive axon collaterals within the neostriatum boutons along these collaterals were found to form symmetrical synaptic contacts. The second kind (type II) of immunoreactive cell body was also of medium-size and had a round or oval shape, but the nucleus was deeply indented and was surrounded by a thin rim of cytoplasm. Synaptic input to this neuron was sparse and consisted of small boutons that made symmetrical contacts with the perikaryon and proximal dendrites.

Many immunoreactive dot-like structures could be seen in the light microscope: upon examination in the electron microscope these were found to be boutons. All fifty-six synaptic boutons that were studied made symmetrical synaptic contacts. These boutons were indistinguishable from the boutons of axon collaterals of identified type I immunoreactive neurons. The most common postsynaptic structures were dendrites, including some dendritic spines, although synapses between immunoreactive boutons and several perikarya, and an axon initial segment were observed. The morphological features of the immunoreactive boutons in the neostriatum were very similar to one type of substance P-immunoreactive bouton in the substantia nigra and to a bouton type in the substantia nigra which is labelled following the anterograde transport of horseradish peroxidase from the striatum.

It is suggested that there are two kinds of substance P-containing neurons in the striatum and that one of these is likely to belong to the medium-spiny class. The latter type of neuron is probably the source of the striatonigral substance P-containing projection and of the immunoreactive boutons within the striatum. The finding of substance P-immunoreactive synaptic boutons within the neostriatum provides a morphological basis for the view that substance P might serve as a neurotransmitter in the neostriatum.

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.

Similar content being viewed by others

References

  • Bak, I. J., Markham, C. H., Cook, M. L. &Stevens, J. G. (1978) Ultrastructural and immunoperoxidase study of striatonigral neurons by means of retrograde axonal transport of Herpes simplex virus.Brain Research 143, 361–9.

    Google Scholar 

  • Ben-Ari, Y., Pradelles, P. &Dray, F. (1979) Identification of authentic substance P in striatonigral and amygdaloid nuclei using combined high performance liquid chromatography and radioimmunoassay.Brain Research 173, 360–3.

    Google Scholar 

  • Bishop, G. A., Chang, H. T. &Kitai, S. T. (1982) Morphological and physiological properties of neostriatal neurons: an intracellular horseradish peroxidase study in the rat.Neuroscience 7, 179–91.

    Google Scholar 

  • Bolam, J. P., Powell, J. F., Totterdell, S. &Smith, A. D. (1981a) The proportion of neurons in the rat neostriatum that project to the substantia nigra demonstrated using horseradish peroxidase conjugated with wheatgerm agglutinin.Brain Research 220, 339–43.

    Google Scholar 

  • Bolam, J. P., Somogyi, P., Totterdell, S. &Smith, A. D. (1981b) A Second type of striatonigral neuron: a comparison between retrogradely labelled and Golgi-stained neurons at the light and electron microscopic levels.Neuroscience 6, 2141–57.

    Google Scholar 

  • Bolam, J. P., Clarke, D. J., Smith, A. D. &Somogyi, P. (1983) A type of aspiny neuron in the rat neostriatum accumulates [3H]γ-aminobutyric acid: combination of Golgi-staining, autoradiography and electron microscopy.Journal of Comparative Neurology (in press).

  • Buck, S. H., Burks, T. F., Brown, M. R. &Yamamura, H. I. (1981) Reduction in basal ganglia and substantia nigra substance P levels in Huntington's disease.Brain Research 209, 464–9.

    Google Scholar 

  • Chang, H. T., Wilson, C. J. &Kitai, S. T. (1981) Single neostriatal efferent axons in the globus pallidus: a light and electron microscopic study.Science 213, 915–8.

    Google Scholar 

  • Clarke, D. J., Bolam, J. P., Somogyi, P. &Smith, A. D. (1982) Morphological characterization of [3H]GABA-accumulating neurons in the rat neostriatum.Neuroscience 7, Suppl. S41.

  • Cuello, A. C. &Kanazawa, I. (1978) The distribution of substance P-immunoreactive fibres in the rat central nervous system.Journal of Comparative Neurology 178, 129–56.

    Google Scholar 

  • Danner, H. &Pfister, C. (1981) 4 spine-lose Neurontypen im Neostriatum der Ratte.Journal für Hirnforschung 22, 465–77.

    Google Scholar 

  • DiFiglia, M., Pasik, T. &Pasik, P. (1980) Ultrastructure of Golgi-impregnated and gold-toned spiny and aspiny neurons in the monkey neostriatum.Journal of Neurocytology 9, 471–92.

    Google Scholar 

  • DiFiglia, M., Aronin, N. &Martin, J. B. (1982) Light and electron microscopic localization of immunoreactive leu-enkephalin in the monkey basal ganglia.Journal of Neuroscience 2, 303–20.

    Google Scholar 

  • Dimova, R., Vuillet, J. &Seite, R. (1980) Study of the rat neostriatum using a combined Golgi-electron microscope technique and serial sections.Neuroscience 5, 1581–96.

    Google Scholar 

  • Emson, P. C., Arregui, A., Clement-Jones, V., Sanberg, B. E. B. &Rossor, M. (1980) Regional distribution of methionine-enkephalin and substance P-like immunoreactivity in normal human brain and in Huntington's disease.Brain Research 199, 147–60.

    Google Scholar 

  • Frotscher, M., Rinne, U., Hassler, R. &Wagner, A. (1981) Termination of cortical afferents on identified neurons in the caudate nucleus of the cat. A combined Golgi-EM degeneration study.Experimental Brain Research 41, 329–37.

    Google Scholar 

  • Gale, J. S., Bird, E. D., Spokes, E. G., Iversen, L. L. &Jessell, T. (1978) Human brain substance P: distribution in controls and Huntington's chorea.Journal of Neurochemistry 30, 633–4.

    Google Scholar 

  • Henderson, Z. (1981) Ultrastructure and acetylcholinesterase content of neurones forming connections between the striatum and substantia nigra of rat.Journal of Comparative Neurology 197, 185–96.

    Google Scholar 

  • Kanazawa, I., Bird, E., O'Connell, R. &Powell, D. (1977). Evidence for a decrease in substance P content of substantia nigra in Huntington's chorea.Brain Research 120, 387–92.

    Google Scholar 

  • Kanazawa, I., Emson, P. C. &Cuello, A. C. (1977b) Evidence for the existence of substance P-containing fibres in striato-nigral and pallido-nigral pathways in rat brain.Brain Research 119, 447–53.

    Google Scholar 

  • Kanazawa, I., Mogaki, S., Muramoto, O. &Kuzuhara, S. (1980) On the origin of substance P-containing fibres in the entopeduncular nucleus and the substantia nigra of the rat.Brain Research 184, 481–5.

    Google Scholar 

  • Kemp, J. M. &Powell, T. P. S. (1971) The structure of the caudate nucleus of the cat: light and electron microscopy.Philosophical Transactions of the Royal Society of London B 262, 383–401.

    Google Scholar 

  • Le Gal La Salle, G. &Ben-Ari, Y. (1977) Microiontophoretic effects of substance P on neurons of the medial amygdala and putamen of the rat.Brain Research 135, 174–9.

    Google Scholar 

  • Leontovich, T. A. (1954) Fine structure of subcortical ganglia (in Russian),Zhurnal Nevropatologii i Psikhiatrii 54, 168–78.

    Google Scholar 

  • Ljungdahl, A., Hökfelt, T. &Nilsson, G. (1978a) 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 

  • Ljungdahl, A., Hökfelt, T., Nilsson, G. &Goldstein, M. (1978b) Distribution of substance P-like immunoreactivity in the central nervous system of the rat-II. Light microscopic localization in relation to catecholamine-containing neurons.Neuroscience 3, 945–76.

    Google Scholar 

  • Michelot, R., Leviel, V., Torrens, Y., Glowinski, J. &Cheramy, A. (1979).In vivo release of substance P in the cat substantia nigra.Neuroscience Letters 15, 141–6.

    Google Scholar 

  • Nicoll, R. A., Schenker, C. &Leeman, S. E. (1980) Substance P as a transmitter candidate.Annual Review of Neuroscience 3, 227–68.

    Google Scholar 

  • Park, M. R., Lighthall, J. W. &Kitai, S. T. (1980) Recurrent inhibition in the rat neostriatum.Brain Research 194, 359–69.

    Google Scholar 

  • Pasik, P., Pasik, T. &DiFiglia, M. (1979) The internal organization of the neostriatum in mammals. InThe Neostriatum (edited byDivac, I. andÖberg, R. G. E.), pp. 5–36. Oxford: Pergamon Press.

    Google Scholar 

  • Pettibone, D. J., Wurtman, R. J. &Leeman, S. E. (1980) Striatal substance P-like immunoreactivity: characterization by high-performance liquid chromatography and aspects of subcellular distribution and in vitro release by potassium.Life Sciences 27, 1593–602.

    Google Scholar 

  • Pickel, V. M., Sumal, K. K., Beckley, S. C., Miller, R. J. &Reis, D. J. (1980) Immunocytochemical localization of enkephalin in the neostriatum of rat brain: a light and electron microscopic study.Journal of Comparative Neurology 189, 721–40.

    Google Scholar 

  • Sakanaka, M., Shiosaka, S., Takatsuki, K., Inagaki, S., Takagi, H., Senba, E., Kawai, Y., Matsuzaki, T. &Tohyama, M. (1981) Experimental immunohistochemical studies on the amygdalofugal peptidergic (substance P and somatostatin) fibers in the stria terminalis of the rat.Brain Research 221, 231–42.

    Google Scholar 

  • Smith, A. D., Bolam, J. P. &Somogyi, P. (1981) An approach to the identification of neurotransmitters in characterized synapses of complex neuronal networks: application to the basal ganglia of the rat. InChemical Neurotransmission 75years (edited byStjarne, L., Hedqvist, P., Lagercrantz, H. andWennmalm, A.), pp. 463–479. London: Academic Press.

    Google Scholar 

  • Somogyi, P., Bolam, J. P. &Smith, A. D. (1981a) Monosynaptic cortical input and local axon collaterals of identified striatonigral neurons. A light and electron microscopic study using the Golgi-peroxidase transport-degeneration procedure.Journal of Comparative Neurology 195, 567–84.

    Google Scholar 

  • Somogyi, P., Bolam, J. P., Totterdell, S. &Smith, A. D. (1981b) Monosynaptic input from the nucleus accumbens-ventral striatum region to retrogradely labelled nigrostriatal neurones.Brain Research 217, 245–63.

    Google Scholar 

  • Somogyi, P., Hodgson, A. J. &Smith, A. D. (1979) An approach to tracing neuron networks in the cerebral cortex and basal ganglia. Combination of Golgi staining, retrograde transport of horseradish peroxidase and anterograde degeneration of synaptic boutons in the same material.Neuroscience 4, 1805–52.

    Google Scholar 

  • Somogyi, P., Priestley, J. V., Cuello, A. C., Smith, A. D. &Bolam, J. P. (1982a) Synaptic connections of substance P-immunoreactive nerve terminals in the substantia nigra of the rat: a correlated light- and electron-microscopic study.Cell and Tissue Research 223, 469–86.

    Google Scholar 

  • Somogyi, P., Priestley, J. V., Cuello, A. C., Smith, A. D. &Takagi, H. (1982b) Synaptic connections of enkephalin-immunoreactive nerve terminals in the neostriatum: a correlated light and electron microscopic study.Journal of Neurocytology 11, 779–807.

    Google Scholar 

  • Somogyi, P. &Smith, A. D. (1979) Projection of neostriatal spiny neurons to the substantia nigra. Application of a combined Golgi-staining and horseradish peroxidase transport procedure at both light and electron microscopic levels.Brain Research 178, 3–15.

    Google Scholar 

  • Somogyi, P. &Takagi, H. (1982) A note on the use of picric acid-paraformaldehyde-glutar-aldehyde fixative for correlated light and electron microscopic immunocytochemistry.Neuroscience 7, 1779–83.

    Google Scholar 

  • Sperk, G. S. &Singer, E. A. (1982)In vivo synthesis of substance P in the corpus striatum of the rat and its transport to the substantia nigra.Brain Research 238, 127–35.

    Google Scholar 

  • Staines, W. A., Nagy, J. I., Vincent, S. R. &Fibiger, H. C. (1980) Neurotransmitters contained in the efferents of the striatum.Brain Research 194, 391–402.

    Google Scholar 

  • Starr, M. (1978) Investigation of possible interactions between substance P and transmitter mechanisms in the substantia nigra and corpus striatum of the rat.Journal of Pharmacy and Pharmacology 30, 359–63.

    Google Scholar 

  • Wilson, C. J. &Groves, P. M. (1980) Fine structure and synaptic connections of the common spiny neuron of the rat neostriatum: a study employing intracellular injection of horseradish peroxidase.Journal of Comparative Neurology 194, 599–615.

    Google Scholar 

Download references

Author information

Author notes

  1. H. Takagi

    Present address: Department of Neuroanatomy, Institute of Higher Nervous Activity, Osaka University Medical School, 4-3-57 Nakanoshima, Kitaku, Osaka, Japan

Authors and Affiliations

  1. University Department of Pharmacology, South Parks Road, OX1 3QT, Oxford, UK

    J. P. Bolam, P. Somogyi, H. Takagi & A. D. Smith

  2. 1st Department of Anatomy, Semmelweis Medical School, Tüzoltó utca 58, Budapest IX, Hungary

    P. Somogyi, H. Takagi & I. Fodor

Authors
  1. J. P. Bolam
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. Somogyi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. Takagi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. I. Fodor
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. D. Smith
    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

Bolam, J.P., Somogyi, P., Takagi, H. et al. Localization of substance P-like immunoreactivity in neurons and nerve terminals in the neostriatum of the rat: a correlated light and electron microscopic study. J Neurocytol 12, 325–344 (1983). https://doi.org/10.1007/BF01148468

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01148468

Keywords

Search

Navigation