Summary
Substance P-immunoreactive boutons were examined in the electron microscope in sections of the rat neostriatum that contained retrogradely labelled striatonigral neurons and/or Golgi-impregnated medium-size densely spiny neurons. The postsynaptic targets of the immunoreactive boutons were characterized on the basis of ultrastructural features, their projection to the substantia nigra and/or their somato-dendritic morphology. Substance P-immunoreactive axonal boutons formed symmetrical synaptic specializations. Of a total of 233 randomly identified synaptic boutons 72.5% made contact with dendritic shafts, 15% with dendritic spines and 10.7% with perikarya. The ultrastructural characteristics of some of the postsynaptic neuronal perikarya were consistent with their identification as striatal interneurons. Similarly, the observation of some of the substance P-containing terminals in contact with spines, spine-bearing dendritic shafts and perikarya with the ultrastructural characteristics of medium-size densely spiny neurons suggested that one of the targets of substance P-positive terminals are striatal projection neurons. Direct evidence for this was obtained in sections from rats that had received injections of horseradish peroxidase conjugated with wheatgerm agglutinin in the substantia nigra. The perikarya of retrogradely labeled striatonigral neurons were found to receive symmetrical synaptic input from substance P-positive boutons. Ultrastructural analysis of Golgi-impregnated medium-size densely spiny neurons, some of which were also retrogradely labeled from the substantia nigra, demonstrated directly that this class of neuron was postsynaptic to the substance P-immunoreactive boutons. The combination of Golgi-impregnation with substance P-immunocytochemistry made it possible to study the pattern or topography of the substance P-positive input to medium size densely spiny neurons. The substance P-containing boutons made contact predominantly with perikarya and dendritic shafts. This pattern of input is markedly different from that of other identified inputs to medium-size densely spiny neurons.
Similar content being viewed by others
References
Barbeau A, Rondeau DB, Jolicœur FB (1981) Substance P in the control of muscle tone. In: Rose FC, Capildeo R (eds) Research progress in Parkinson's disease. Pitman Medical Press, London, pp 158–164
Beaujouan JC, Torrens Y, Herbert A, Daguet MC, Glowinski J, Prochiantz A (1982) Specific binding of an immunoreactive and biologically active 125I-labeled substance P derivative to mouse mesencephalic cells in primary culture. Molec Pharmacol 22: 48–55
Bolam JP (1984) Synapses of identified neurons in the neostriatum. In: Evered D, O'Connor M (eds) Functions of the basal ganglia. Pitman, London, (Ciba Foundation Symposium 107) pp 30–47
Bolam JP (1987) Substance P and 5HT input to dopamine neurons in the substantia nigra of the rat. Neurosci Lett Suppl 29: S111
Bolam JP, Clarke DJ, Smith AD, Somogyi P (1983a) A type of aspiny neuron in the rat neostriatum accumulates [3H]-γ-aminobutyric acid: combination of Golgi-staining, autoradiography and electron microscopy. J Comp Neurol 213: 121–134
Bolam JP, Ingham CA, Izzo PN, Rye DB, Smith AD, Wainer BH (1986) Substance P-containing terminals in synaptic contact with cholinergic neurons in the neostriatum and basal forebrain: a double immunocytochemical study in the rat. Brain Res 397: 279–289
Bolam JP, Izzo PN (1986) Cholinergic boutons in synaptic contact with striatonigral neurons in the rat neostriatum. Neurosci Lett Suppl 26: S312
Bolam JP, Izzo PN (1987) Possible sites of transmitter-interactions in the neostriatum: an anatomical approach. In: Sandler M, Feuerstein C, Scatton B (eds) Neurotransmitter interactions in the basal ganglia. Raven Press, New York, pp 47–58
Bolam JP, Powell JF, Wu J-Y, Smith AD (1985) Glutamate decarboxylase-immunoreactive structures in the rat neostriatum: a correlated light and electron microscopic study including a combination of Golgi-impregnation with immunocytochemistry. J Comp Neurol 237: 1–20
Bolam JP, Somogyi P, Takagi H, Fodor I, Smith AD (1983b) 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
Bolam JP, Somogyi P, Totterdell S, Smith AD (1981) A second type of striatonigral neuron: a comparison between retrogradely labelled and Golgi-stained neurons at the light and electron microscopic levels. Neuroscience 6: 2141–2157
Bolam JP, Wainer BH, Smith AD (1984) Characterization of cholinergic neurons in the rat neostriatum. A combination of choline acetyltransferase immunocytochemistry, Golgi-impregnation and electron microscopy. Neuroscience 12: 711–718
Chang HT, Wilson CJ, Kitai ST (1981) Single neostriatal efferent axons in the globus pallidus: a light and electron microscopic study. Science 213: 915–918
Chang HT, Wilson CJ, Kitai ST (1982) A Golgi study of rat neostriatal neurons: light microscopic analysis. J Comp Neurol 208: 107–126
Chung JW, Hassler R, Wagner A (1977) Degeneration of two of nine types of synapses in the putamen after center median coagulation in the cat. Exp Brain Res 28: 345–362
Cuello AC, Galfre G, Milstein C (1979) Detection of substance P in the central nervous system by a monoclonal antibody. Proc Natl Acad Sci USA 76: 3532–3536
Davies J, Dray A (1976) Substance P in the substantia nigra. Brain Res 107: 623–627
Del Rio J, Naranjo JR, Yang H-Y, Costa T (1983) Substance P-induced release of met5-enkephalin from striatal and periaqueductal gray slices. Brain Res 279: 121–126
DiFiglia M (1987) Synaptic organization of cholinergic neurons in the monkey neostriatum. J Comp Neurol 255: 245–258
DiFiglia M, Aronin N (1982) Ultrastructural features of immunoreactive somatostatin neurons in the rat caudate nucleus. J Neurosci 2: 1267–1274
DiFiglia M, Aronin N (1986) Light and electron microscopic localization of immunoreactive substance P in the monkey neostriatum. Soc Neurosci Abstr 12: 1328
DiFiglia M, Pasik T, Pasik P (1980) Ultrastructure of Golgi-impregnated and gold-toned spiny and aspiny neurons in the monkey neostriatum. J Neurocytol 9: 471–492
Dimova R, Vuillet J, Seite R (1980) Study of the rat neostriatum using a combined Golgi-electron microscope technique and serial sections. Neuroscience 5: 1581–1596
Dubé L, Bolam JP, Smith AD (1985) Identification of synaptic terminals of thalamic or cortical origin in contact with distinct medium size spiny neurons in the rat neostriatum. J Comp Neurol (in press)
Freund TF, Powell JF, Smith AD (1984) Tyrosine hydroxylase-immunoreactive synaptic boutons in contact with identified striatonigral neurons, with particular reference to dendritic spines. Neuroscience 13: 1189–1215
Freund TF, Somogyi P (1983) The section-Golgi impregnation procedure. I. Description of the method and its combination with histochemistry after intracellular iontophoresis or retrograde transport of horseradish peroxidase. Neuroscience 9: 463–474
Frotscher M, Rinne U, Hassler R, Wagner A (1981) Termination of cortical afferents on identified neurons in the caudate nucleus of the cat. Exp Brain Res 41: 329–337
Graybiel AM, Ragsdale CW (1983) Biochemical anatomy of the striatum. In: Emson PC (eds) Chemical neuroanatomy. Raven Press, New York, pp 427–504
Haber SN, Nauta WJH (1983) Ramifications of the globus pallidus in the rat as indicated by patterns of immunohistochemistry. Neuroscience 9: 245–260
Hall ME, Grantham PA, Stewart JM (1985) Age and strain differences in some behavioral effects of intracranial substance P. Peptides 6: 363–368
Herrera-Marschitz M, Christensson-Nylander I, Sharp T, Staines W, Reid M, Hökfelt T, Terenius L, Ungerstedt U (1986) Striato-nigral dynorphin and substance P pathways in the rat. II. Functional analysis. Exp Brain Res 64: 193–207
Izzo PN, Bolam JP (1986) The postsynaptic targets of substance P-immunoreactive boutons in the rat neostriatum. Neurosci Lett Suppl 26: S312
Izzo PN, Graybiel AM, Bolam JP (1987) Characterization of substance P- and [met]enkephalin-immunoreactive neurons in the caudate nucleus of cat and ferret by a single section Golgi procedure. Neuroscience 20: 577–587
James TA, Starr MS (1979) Effects of substance P injected into the substantia nigra. Br J Pharmacol 65: 423–429
Jolicœur FB, Rondeau DB, Belanger F, Fouriezos G, Barbeau A (1980) Influence of substance P on the behavioural changes induced by haloperidol in rats. Peptides 1: 103–107
Kawai Y, Takagi H, Kumoi Y, Shiosaka S, Tohyama M (1987) Nigrostriatal dopamine neurons receive substance P-ergic inputs in the substantia nigra: application of the immuno electron microscopic mirror technique to fluorescent doublestaining for transmitter-specific projections. Brain Res 401: 371–376
Kelley AE, Iversen SD (1978) Behavioral response to bilateral injections of substance P into the substantia nigra of the rat. Brain Res 158: 474–478
Kemp JM, Powell TPS (1971) The site of termination of afferent fibres in the caudate nucleus. Phil Trans R Soc Ser B 262: 413–427
Kohno J, Shiosaka S, Shinoda K, Inagaki S, Tohyama M (1984) Two distinct strio-nigral substance P pathways in the rat: an experimental immunohistochemical study. Brain Res 308: 309–317
König JFR, Klippel RA (1963) The rat brain. A stereotaxic atlas of the forebrain and lower parts of the brainstem. Williams and Wilkens, Baltimore
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 Res 135: 174–179
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
Michelot R, Leviel V, Torrens Y, Glowinski J, Cheramy A (1979) In vivo release of substance P in the cat substantia nigra. Neurosci Lett 15: 135–141
Olpe H-R, Koella WP (1977) Rotatory behavior in rats by intranigral application of substance P and an eledosin fragment. Brain Res 126: 576–579
Penny GR, Afsharpoor S, Kitai ST (1986) The glutamate decarboxylase-leucine enkephalin-, methionine enkephaline- and substance P-immunoreactive neurons in the neostriatum of the rat and cat: evidence for partial population overlap. Neuroscience 17: 1011–1045
Petit F, Glowinski J (1986) Stimulatory effect of substance P on the spontaneous release of newly synthesized [3H] dopamine from rat striatal slices: a tetrodotoxin-sensitive process. Neuropharmacology 25: 1015–1021
Pettibone DJ, Wurtman RJ, Leeman SE (1980) Striatal substance P-like immunoreactivity: characterization by high-performance liquid chromatography and aspects of subcellular distribution and in vitro release by potassium. Life Sci 27: 1593–1602
Phelps PE, Houser CR, Vaughn JE (1985) Immunocytochemical localization of choline acetyltransferase within the rat neostriatum: a correlated light and electron microscopic study of cholinergic neurons and synapses. J Comp Neurol 238: 286–307
Phelps PE, Vaughn JE (1986) Immunocytochemical localization of choline acetyltransferase in rat ventral striatum: a light and electron microscopic study. J Neurocytol 15: 595–617
Pinnock RD, Woodruff GN, Turnbull MJ (1983) Actions of substance P, MIF, TRH and related peptides in the substantia nigra, caudate nucleus and nucleus accumbens. Neuropharmacology 22: 687–696
Ritter JK, Gehlert DR, Gibb JW, Wamsley JK, Hanson GR (1985) Neuronal localization of substance P receptors in rat neostriatum. Eur J Pharmacol 109: 431–432
Somogyi P, Bolam JP, Smith AD (1981) Monosynaptic cortical input and local axon collaterals of identified striatonigral neurons. A light and electron microscopic study using the Golgi-peroxidase transport-degeneration procedure. J Comp Neurol 195: 567–584
Somogyi P, Priestly JV, Cuello AC, Smith AD, Bolam JP (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 Res 223: 469–486
Somogyi P, Priestly JV, Cuello AC, Smith AD, Takagi H (1982b) Synaptic connections of enkephalin-imrmmoreactive nerve terminals in the neostriatum: a correlated light and electron microscopic study. J Neurocytol 11: 779–807
Somogyi P, Smith AD (1979) Projection of neostriatal spiny neurons to the substantia nigra. Applications of a combined Golgi-staining and horseradish peroxidase transport procedure at both light and electron microscopic levels. Brain Res 178: 3–15
Starr MS (1982) Influence of peptides on 3H-dopamine release from superfused rat striatal slices. Neurochem Int 4: 233–240
Sugimoto T, Takada M, Kaneko T, Mizuno N (1984) Substance P positive thalamocaudate neurons in the center median-parafascicular complex in the cat. Brain Res 323: 181–184
Takagi H, Somogyi P, Smith AD (1984) Aspiny neurons and their local axons in the neostriatum of the rat: a correlated light and electron microscopic study of Golgi-impregnated material. J Neurocytol 13: 239–265
Takagi H, Somogyi P, Somogyi J, Smith AD (1983) Fine structural studies on a type of somatostatin-immunoreactive neuron and its synaptic connections in the rat neostriatum: a correlated light and electron microscopic study. J Comp Neurol 214: 1–16
Torrens Y, Beaujouan JC, Viger A, Glowinski J (1983) Properties of a 125I-substance P derivative binding to synaptosomes from various brain structures and the spinal cord of the rat. Naunyn Schmiedebergs Arch Pharmacol 324: 134–139
Walker RJ, Kemp JA, Yajima H, Kitagawa K, Woodruff GN (1976) The action of substance P on mesencephalic reticular and substantia nigra neuron of the rat. Experientia 32: 214–215
Wilson CJ, Groves PM (1980) Fine structure and synaptic connections of the common spiny neuron of the rat neostriatum: a study employing intra cellular injection of horseradish peroxidase. J Comp Neurol 194: 599–615
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Bolam, J.P., Izzo, P.N. The postsynaptic targets of substance P-immunoreactive terminals in the rat neostriatum with particular reference to identified spiny striatonigral neurons. Exp Brain Res 70, 361–377 (1988). https://doi.org/10.1007/BF00248361
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00248361