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Striato-nigral dynorphin and substance P pathways in the rat

I. Biochemical and immunohistochemical studies

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Summary

The effect of striatal ibotenic acid lesions on dynorphin-, substance P- and enkephalin-like immunoreactivities in the substantia nigra has been studied with immunohistochemistry as well as biochemistry. A comparison was made with the effects produced by intranigral ibotenic acid lesion and by 6-hydroxy-dopamine injection into the medial forebrain bundle. In addition, the effect of the striatal lesions on nigral glutamic acid decarboxylase (GAD)-positive structures was analysed with immunohistochemistry. The effect of the lesions was analysed functionally in the Ungerstedt rotational model, in order to obtain a preliminary evaluation of the extent of the lesions. The striatal lesions produced a parallel depletion of dynorphin and substance P levels in the substantia nigra, pars reticulata, ipsilateral to the treated side, which was dependent upon the extent and location of the lesion. Ibotenic acid lesions into the tail and the corpus of the striatum produced stronger nigral-peptide depletion than lesions in the head and the corpus of the striatum. Comparison of placement of lesions and localization of depleted area in the substantia nigra revealed a topographical relationship. Furthermore, the nigral depletion patterns of dynorphin and substance P were similar. The immunohistochemical analysis revealed that also GAD-positive fibers in the pars reticulata to a large extent disappeared after striatal lesions, in parallel to the dynorphin- and substance P-positive fibers. However, the depletion was less pronounced for GAD than for the peptides, probably related to presence of local GABA neurons in the zona reticulata of the substantia nigra. These results indicate that with the types of lesion used in this study it is not possible to provide evidence for a differential localization within the striatum of dynorphin-, substance P- and GABA-positive cell bodies projecting to the substantia nigra. The radioimmunoassay showed that (Leu)- but not (Met)-enkephalin was affected to the same extent as the dynorphin peptides, supporting the view that (Leu)-enkephalin in the pars reticulata of the substantia nigra is derived from proenkephalin B and not from proenkephalin A. In the immunohistochemical analysis (Met)-enkephalin-like immunoreactivity could only be detected in the pars compacta of the substantia nigra and did not seem to be affected by any of the lesions. The striatal lesions produced a behavioural asymmetry, which could be disclosed by stimulating the rats with apomorphine, which produced ipsilateral rotation. The total number and intensity of the rotation were closely correlated to the extent and location of the striatal lesion as well as to the amount of dynorphin and substance P depletion found in the substantia nigra of the treated side. The results provide further evidence for the presence of a dynorphin-containing system with fibers originating mainly in the corpus and tail of the striatum and terminating in the zona reticulata of the substantia nigra and may, similarly to the previously characterized substance P and GABA containing pathways, have a role in the control of motor behaviour.

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References

  • Anden N-E, Dahlström A, Fuxe K, Larsson K, Olson L, Ungerstedt U (1966) Ascending monoamine neurons to the telencephalon and diencephalon. Acta Physiol Scand 67: 313–326

    Google Scholar 

  • Aronin N, DiFiglia M, Graveland GA, Schwartz WJ, Wu J-Y (1984) Localization of immunoreactive enkephalins in GABA synthesizing neurons of the rat neostriatum. Brain Res 300: 376–380

    Google Scholar 

  • Bergström L, Christensson I, Folkesson F, Stenström B, Terenius L (1983) An ion exchange chromatography and radioimmunoassay procedure for measuring opioid peptides and substance P. Life Sci 33: 1613–1619

    Google Scholar 

  • Bolam JP, Somogyi P, Totterdell S, Smith AD (1981a) A second type of striatonigral neuron: a comparison between retrogradely labeled and Golgi-stained neurons at the light and electron microscopic levels. Neuroscience 6: 2141–2157

    Google Scholar 

  • Bolam JP, Powell JF, Totterdell S, Smith AD (1981b) The proportion of neurons in the rat neostriatum that project to the substantia nigra demonstrated using horseradish peroxide conjugated with wheat-germ agglutinin. Brain Res 220: 339–343

    Google Scholar 

  • Bolam JP, Clarke DJ, Smith AD, 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. J Comp Neurol 213: 121–134

    Google Scholar 

  • 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

    Google Scholar 

  • Brownstein MJ, Mroz MJ, Mroz EA, Tappaz ML, Leeman SE (1977) On the origin of substance P and glutamic decarboxylase (GAD) in the substantia nigra. Brain Res 135: 315–323

    Google Scholar 

  • Christensson-Nylander I, Terenius L (1985) Dynorphin peptides in the human substantia nigra. Neuropeptides 6: 391–396

    Google Scholar 

  • Christensson-Nylander I, Nyberg F, Ragnarsson U, Terenius L (1985) A general procedure for analysis of proenkeph'alin B derived opioid peptides. Regul Pept 11: 65–76

    Google Scholar 

  • Comb M, Seeburg PH, Adelman J, Eiden L, Herbert E (1982) Primary structure of the human Met- and Leu-enkephalin precursor and its mRNA. Nature 295: 663–666

    Google Scholar 

  • Coons AH (1958) Fluorescent antibody methods. In: Danielli JF (ed) General cytochemical methods. Academic Press, New York, pp 339–422

    Google Scholar 

  • Correa FMA, Innis RB, Hester LD, Snyder SH (1981) Diffuse enkephalin innervation from caudate to globus pallidus. Neurosci Lett 25: 63–68

    Google Scholar 

  • Cuello AC, Kanazawa I (1978) The distribution of substance P immunoreactive fibers in the rat central nervous system. JComp Neurol 178: 129–150

    Google Scholar 

  • Cuello AC, Paxinos G (1978) Evidence for a long leu-enkephalin striopallidal pathway in rat brain. Nature 271: 178–180

    Google Scholar 

  • Cuello AC, Kanazawa I (1978) The distribution of substance P immunoreactive fibers in the rat central nervous system. JComp Neurol 178: 129–156

    Google Scholar 

  • 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

    Google Scholar 

  • Dahlström A, Fuxe K (1964) Evidence for the existence of monoamine-containing neurons in the central nervous system. I. Demonstration of monoamine in the cell bodies of the brain stem neurons. Acta Physiol Scand 62 (Suppl 232): 1–55

    Google Scholar 

  • Del Fiacco M, Paxinos G, Cuello AC (1982) Neostriatal enkephalin-immunoreactive neurons project to the globus pallidus. Brain Res 231: 1–17

    Google Scholar 

  • DiCarlo V, Hubbard JE, Pate P (1973) Fluorescence histochemistry of monoamine-containing cell bodies in the brainstem of the squirrel monkey (Saimiri sciureus) IV. An atlas. J Comp Neurol 152: 347–372

    Google Scholar 

  • Dores RM, Lewis ME, Khachaturian H, Watson SJ, Akil H (1985) Analysis of opioid and non-opioid end products of prodynorphin in the substantia nigra of the rat. Neuropeptides 5: 501–504

    Google Scholar 

  • Elde R, Hökfelt T, Johansson O, Terenius L (1976) Immunohistochemical studies using antibodies to leucine-enkephalin: initial observations on the nervous system of the rat. Neuroscience 1: 349–351

    Google Scholar 

  • Emson PC, Arrequi A, Clement V-J, Sandberg BEB, Rossor M (1980) Regional distribution of methionine-enkephalin and substance P-like immunoreactivity in normal human brain and in Huntington's disease. Brain Res 199: 147–160

    Google Scholar 

  • Fallon JH, Leslie FM, Cone RI (1985) Dynorphin-containing pathways in the substantia nigra and ventral tegmentum: double labeling study using combined immunofluorescence and retrograde tracing. Neuropeptides 5: 457–460

    Google Scholar 

  • Finley JCW, Maderdrut JL, Petrusz P (1981) The immunocytochemical localization of enkephalin in the central nervous system. J Comp Neurol 198: 541–565

    Google Scholar 

  • Fonnum F, Grofova I, Rinvik E, Storm-Mathisen J, Walberg F (1974) Origin and distribution of glutamate decarboxylase in substantia nigra of the cat. Brain Res 71: 77–92

    Google Scholar 

  • Fonnum F, Gottesfeld Z, Grofova I (1978) Distribution of glutamate decarboxylase, choline acetyl-transferase and aromatic amino acid decarboxylase in the basal ganglia of normal and operated rats. Evidence for striatopallidal, striatoentopenduncular and striatonigral GABA-ergic fibres. Brain Res 143: 125–138

    Google Scholar 

  • Gale K, Hong JS, Guidotti A (1977) Presence of substance P and GABA in separate striatonigral neurons. Brain Res 136: 371–375

    Google Scholar 

  • Gale K, Casu M (1981) Dynamic utilization of GABA in substantia nigra: regulation by dopamine and GABA in the striatum, and its clinical and behavioural implications. Mol Cell Biochem 39: 369–405

    Google Scholar 

  • Gaspar P, Berger B, Gay M, Hamon M, Cesselin F, Vigny A, Javoy-Agid F, Agid Y (1983) Tyrosine hydroxylase and methionine-enkephalin in the humane mesencephalon. J Neurol Sci 58: 247–267

    Google Scholar 

  • Gerfen CR (1985) The neostriatal mosaic. I. Compartmental organization of projections from the striatum to the substantia nigra in the rat. J Comp Neurol 236: 454–476

    Google Scholar 

  • Gerfen CR, Staines WA, Arbuthnott GW, Fibiger HC (1982) Crossed connections of the substantia nigra in the rat. J Comp Neurol 207: 283–303

    Google Scholar 

  • Goldstein A, Tachibana S, Lowney LI, Hunkapiller M, Hood L (1979) Dynorphin-(1–13), an extraordinarily potent opioid peptide. Proc Natl Acad Sci USA 76: 6666–6670

    Google Scholar 

  • Goldstein A, Fischli W, Lowney LI, Hunkapiller M, Hood L (1981) Porcine pituitary dynorphin: complete amino acid sequence of the biologically active heptadecapeptide. Proc Natl Acad Sci USA 78: 7219–7223

    Google Scholar 

  • Gramsch C, Höllt V, Mehraein P, Pasi A, Herz A (1979) Regional distribution of methionine-enkephalin- and β-endorphinlike immunoreactivity in human brain and pituitary. Brain Res 171: 261–270

    Google Scholar 

  • Gramsch C, Höllt V, Pasi A, Mehraein P, Herz A (1982) Immunoreactive dynorphin in human brain and pituitary. Brain Res 233: 65–74

    Google Scholar 

  • Graybiel AM, Ragsdale CW (1983) Biochemical anatomy of the striatum. In: PC Emson (ed) Chemical neuroanatomy. Raven Press, New York, pp 427–504

    Google Scholar 

  • Grofova I (1979) Extrinsic connections of the neostriatum. In: Divac I, Oberg RGE (eds) The neostriatum. Pergamon Press, Oxford, pp 37–51

    Google Scholar 

  • Haber S, Elde R (1982) The distribution of enkephalin immunoreactive fibers and terminals in the monkey central nervous system: an immunohistochemical study. Neuroscience 7: 1049–1095

    Google Scholar 

  • Hanson GR, Alphs L, Wolf W, Levine R, Lovenber W (1981) Haloperidol-induced reduction of nigral substance P-like immunoreactivity: a probe for the interaction between dopamine and substance P neuronal systems. J Pharmacol Exp Ther 218: 568–574

    Google Scholar 

  • Hartman BK (1973) Immunofluorescence of dopamine-β-hydroxylase. Application of improved methodology to the localization of the peripheral and central noradrenergic nervous system. J Histochem Cytochem 4: 312–332

    Google Scholar 

  • Hattori T, McGeer PL, Fibiger HC, McGeer EG (1973) On the source of GABA-containing terminals in the substantia nigra. Electron microscopic autoradiographic and biochemical studies. Brain Res 54: 103–114

    Google Scholar 

  • Herrera-Marschitz M, Hökfelt T, Ungerstedt U, Terenius L (1983) Functional studies with the opioid peptide dynorphin: acute effects of injections into the substantia nigra reticulata of naive rats. Life Sci 33 (Suppl 1): 555–558

    Google Scholar 

  • Herrera-Marschitz M, Ungerstedt U (1984a) Evidence that apomorphine and pergolide induce rotation in rats by different actions on D1 and D2 receptor sites. Eur J Pharmacol 98: 165–176

    Google Scholar 

  • Herrera-Marschitz M, Ungerstedt U (1984b) Evidence that striatal efferents relate to different dopamine receptor. Brain Res 323: 269–278

    Google Scholar 

  • Herrera-Marschitz M, Hökfelt T, Ungerstedt U, Terenius L, Goldstern M (1984) Effect of intranigral injections of dynorphin, dynorphin fragments and α-neoendorphin on rotational behaviour in the rat. Eur J Pharmacol 102: 213–227

    Google Scholar 

  • 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

    Google Scholar 

  • Hong JS, Yang HY, Racagni G, Costa E (1977) Projections of substance P containing neurons from neostriatum to substantia nigra. Brain Res 122: 541–544

    Google Scholar 

  • Hökfelt T, Ungerstedt U (1973) Specificity of 6-hydroxydopamine induced degeneration of central monoamine neurons: an electron and fluorescence microscopic study with special reference to intracerebral injection on the nigro-striatal dopamine system. Brain Res 60: 269–297

    Google Scholar 

  • Hökfelt T, Fuxe K, Goldstein M, Job TH (1973) Immunohistochemical studies of three catecholamine synthesizing enzymes: aspects on methodology. Histochemistry 33: 231–254

    Google Scholar 

  • Hökfelt T, Johansson O, Goldstein M (1984a) Chemical anatomy of the brain. Science 225: 1326–1334

    Google Scholar 

  • Hökfelt T, Vincent SR, Dalsgaard CJ, Herrera-Marschitz M, Ungerstedt U, Schultzberg M, Christensson I, Terenius L (1984b) Some aspects on distribution and role of opioid peptides in the central and peripheral nervous system. In: Müller EE, Genazzani AP (eds) Central and peripheral endorphins: basic and clinical aspects. Raven Press, New York, pp 1–16

    Google Scholar 

  • Inagaki S, Parent A (1984) Distribution of substance P and enkephalin-like immunoreactivity in the substantia nigra of rat, cat and monkey. Brain Res Bull 13: 319–329

    Google Scholar 

  • James TA, Starr MS (1979) Effects of substance P injected into the substantia nigra. Br J Pharmacol 65: 423–429

    Google Scholar 

  • Jessell TM, Emson PC, Paxinos G, Cuello AC (1978) Topographic projections of substance P and GABA pathways in the striato- and pallido-nigral system: a biochemical and immunohistochemical study. Brain Res 152: 487–509

    Google Scholar 

  • Johnson DG, De Nogueira C, Araujo GM (1981) A simple method of reducing the fading of immunofluorescence during microscopy. J Immunol Meth 43: 349

    Article  CAS  PubMed  Google Scholar 

  • Kakidani H, Furutani Y, Takahashi H, Noda M, Morimoto Y, Hirose T, Asai M, Inayama S, Nakanishi S, Numa S (1982) Cloning and sequence analysis of cDNA for porcine α- neoendorphin/dynorphin precursor. Nature 298: 245–249

    Google Scholar 

  • Kanazawa I, Emson PC, Cuello C (1977) Evidence for the existence of substance P containing fibers in striato-nigral and pallido-nigral pathways in rat brain. Brain Res 119: 447–453

    Google Scholar 

  • Kelley AE, Iversen SD (1979) Substance P infusion into substantia nigra of the rat: behavioural analysis and involvement of striatal dopamine. Eur J Pharmacol 60: 171–179

    Google Scholar 

  • Khachaturian H, Watson SJ, Lewis ME, Coy D, Goldstein A, Akil H (1982) Dynorphin immunocytochemistry in the rat central nervous system. Peptides 3: 941–954

    Google Scholar 

  • Khachaturian H, Lewis ME, Watson SJ (1983) Enkephalin systems in diencephalon and brainstem of the rat. J Comp Neurol 220: 310–320

    Google Scholar 

  • Kim JS, Bak IJ, Hassler R, Okada Y (1971) Role of aminobutyric acid (GABA) in the extrapyramidal motor system. 2. Some evidence for the existence of a type of GABA-rich strionigral neurons. Exp Brain Res 14: 94–104

    Google Scholar 

  • 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

    Google Scholar 

  • König JFR, Klippel RA (1963) The rat brain. A stereotaxic atlas of the forebrain and lower parts of the brain stem. RE Krieger Publishing Co Inc, New York

    Google Scholar 

  • Lindgren S, Anden N-E (1985) Effect of the normal nerve impulse flow on the synthesis and utilization of GABA in the rat substantia nigra. J Neural Transmission 61: 21–34

    Google Scholar 

  • Lindvall O, Björklund A (1974) The organization of the ascending catecholamine neuron systems in the rat brain as revealed by the glyoxylic acid fluorescence method. Acta Physiol Scand Suppl 412: 1–48

    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

    Article  CAS  PubMed  Google Scholar 

  • Ljungdahl A, Hökfelt T, Nilsson G, Goldstein M (1978b) Distribution of substance P-like immunoreactivity in the central nervous system in the rat. II. Light microscopic localization in relation to catecholamine-containing neurons. Neuroscience 3: 945–976

    Google Scholar 

  • Lundberg JM, Hökfelt T, Änggard A, Terenius L, Markey K, Goldstein M (1982) Organization principles in the peripheral sympathetic nervous system: subdivisions by coexisting peptides (somatostatin, avian pancreatic polypeptide and vasoactive intestinal polypeptide-like immunoreactive materials). Proc Natl Acad Sci USA 79: 1300–1307

    Google Scholar 

  • Markey KA, Kondo S, Shenkman L, Goldstein M (1980) Purification and characterization of tyrosine hydroxylase from a clonal pheochromocytoma cell line. Mol Pharmacol 17: 79–85

    Google Scholar 

  • Marshall PE, Landis DD, Zalneraitis EL (1983) Immunocytochemical studies of substance P and leucine-enkephalin in Huntington's disease. Brain Res 289: 11–26

    Google Scholar 

  • Maysinger D, Höllt V, Seizinger BR, Mehraein P, Pasi A, Herz A (1982) Parallel distribution of immunoreactive α-neoendophorin and dynorphin in rat and human tissue. Neuropeptides 2: 211–225

    Google Scholar 

  • McGeer EG, Staines WA, McGeer PL (1984) Neurotransmitters in the basal ganglia. Can J Neurol Sci 11 (Suppl): 89–99

    Google Scholar 

  • Morelli M, Di Chiara G (1985) Non-dopaminergic mechanisms in the turning behaviour evoked by intranigral opiates. Brain Res 341: 350–359

    Google Scholar 

  • Mugnaini E, Oertel WH (1985) An atlas of the distribution of GABAergic neurons and terminals in the rat CNS as revealed by GAD immunohistochemistry. In: Björklund A, Hökfelt T (eds) Handbook of chemical neuroanatomy. Part I, Vol. 4. GABA and neuropeptides in the CNS. Elsevier Science Publishers BV, New York, pp 436–608

    Google Scholar 

  • Nagy JI, Vincent SR, Lehmann J, Fibiger HC, McGeer EG (1978) The use of kainic acid in the localization of enzymes in the substantia nigra. Brain Res 149: 431–441

    Google Scholar 

  • Nauta WJH, Mehler WR (1966) Projections of the lentiform nucleus in the monkey. Brain Res 1: 3–42

    Google Scholar 

  • Nauta WSH, Smitz GP, Faull RC, Domesick VB (1978) Efferent connections and nigral afferents of the nucleus accumbens of the rat. Neuroscience 3: 385–401

    Google Scholar 

  • Noda M, Furutani Y, Takahashi H, Toyosato M, Hirose T, Inayama S, Nakanishi S, Numa S (1982) Cloning and sequence analysis of cDNA for bovine adrenal preproenkephalin. Nature 295: 202–208

    Google Scholar 

  • Oblin A, Zivkovic B, Bartholini G (1984) Involvement of the D-2 dopamine receptor in the neuroleptic-induced decrease in nigral substance P. Eur J Pharmacol 105: 175–177

    Google Scholar 

  • Oertel WH, Schmechel DE, Tappaz ML, Kopin IJ (1981a) Production of a specific antiserum to rat brain glutamic acid decarboxylase by injection of an antigen-antibody complex. Neuroscience 6: 2689–2700

    Google Scholar 

  • Oertel WH, Schmechel DE, Brownstein MJ, Tappaz ML, Ransom DH, Kopin IJ (1981b) Decrease of glutamate decarboxylase (GAD) immunoreactive nerve terminals after kainic acid lesion of the striatum. J Histochem Cytochem 29: 977–980

    Google Scholar 

  • Oertel WH, Tappaz ML, Berod A, Mugnaini (1982) Two-colour immunohistochemistry for dopamine and GABA neurons in rat substantia nigra and zona incerta. Brain Res Bull 9: 463–474

    Google Scholar 

  • Oertel WH, Riethmuller G, Mugnaini E, Schmechel DE, Weindl A, Gramsch C, Herz A (1983) Opioid peptide like immunoreactivity in GABAergic neurons of rat neostriatum and central amygdaloid nucleus. Life Sci 33 (Suppl I): 76–79

    Google Scholar 

  • Oertel WH, Mugnaini E (1984) Immunocytochemical studies of GABAergic neurons in rat basal ganglia and their relations to other neuronal systems. Neurosci Lett 47: 233–238

    Google Scholar 

  • Palkovits M, Brownstein MJ, Zamir N (1984) On the origin of dynorphin A and α-neo-endorphin in the substantia nigra. Neuropeptides 4: 193–199

    Google Scholar 

  • Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates. Academic Press, New York

    Google Scholar 

  • Pearse AGE, Polak JM (1975) Bifunctional reagents as vapour and liquid-phase fixatives for immunohistochemistry. Histochemistry J 7: 179–186

    Google Scholar 

  • Petrusz P, Merchenthaler I, Maderdrut JL (1985) Distribution of enkephalin-containing neurons in the central nervous system. In: Björklund A, Hökfelt T (eds) Handbook of chemical neuroanatomy. Part I, Vol. 4. GABA and neuropeptides in the CNS. Elsevier Science Publishers BV, New York, pp 273–334

    Google Scholar 

  • Pioro EPJ, Hughes JT, Cuello AC (1984) Loss of substance P and enkephalin immunoreactivity in the human substantia nigra after striatopallidal infarction. Brain Res 292: 339–347

    Google Scholar 

  • Pittius CW, Seizinger BR, Pasi A, Mehraein P, Herz A (1984) Distribution and characterization of opioid peptides derived from proenkephalin A in human and rat central nervous system. Brain Res 304: 127–136

    Google Scholar 

  • Platt JL, Michael AF (1983) Retardation of fading and enhancement of intensity of immunofluorescence by P-phenylenediamine. J Histochem Cytochem 31: 840–842

    Google Scholar 

  • Poirier LJ, Langelier P, Roberge A, Boucher R, Kitsikisa A (1972) Non-specific histopathological changes induced by the intracerebral injection of 6-hydroxy-dopamine (6-OH-DA). J Neurol Sci 16: 401–416

    Google Scholar 

  • Poitras D, Parent A (1978) Atlas of distribution of monoaminecontaining nerve cell bodies in the brain stem of the cat. J Comp Neurol 179: 699–718

    Google Scholar 

  • Ribak CE, Vaughn JE, Roberts E (1979) The GABA neurons and their axon terminals in rat corpus striatum as demonstrated by GAD immunocytochemistry. J Comp Neurol 187: 261–284

    Google Scholar 

  • Ribak CE, Vaughn JE, Roberts E (1980) GABAergic nerve terminals decrease in the substantia nigra following hemitransections of the striatonigral and pallidonigral pathways. Brain Res 192: 413–420

    Google Scholar 

  • Royce GJ, Laine EJ (1984) Efferent connections of the caudate nucleus, including cortical projections of the striatum and other basal ganglia: an autoradiographic and horseradish peroxidase investigation in the cat. J Comp Neurol 226: 28–49

    Google Scholar 

  • Sar M, Stumpf WE, Miller RJ, Change KJ, Cuatrecasas P (1978) Immunohistochemical localization of enkephalin in rat brain and spinal cord. J Comp Neurol 182: 17–38

    Google Scholar 

  • Schwarcz R, Hökfelt T, Fuxe K, Jonsson G, Goldstein M, Terenius L (1979) Ibotenic acid-induced neuronal degeneration: a morphological and neurochemical study. Exp Brain Res 37: 199–216

    Google Scholar 

  • Schultzberg M, Hökfelt T, Terenius L, Elfvin L-G, Lundberg JM, Brandt J, Elde RP, Goldstein M (1979) Enkephalin immunoreactive nerve fibers and cell bodies in sympathetic ganglia of the guinea-pig and rat. Neuroscience 4: 249–270

    Google Scholar 

  • Senba E, Shiosaka S, Hara Y, Inagaki S, Kawai Y, Takatsuki K, Sakanaka M, Iida H, Takagi H, Minagawa H, Tohyama M (1982) Ontogeny of the leucine-enkephalin neuron system of the rat. J Comp Neurol 205: 341–359

    Google Scholar 

  • Somogyi P, Bolam JP, Totterdell S, Smith AD (1981) Monosynaptic input from the nucleus accumbens-ventral striatum region to retrogradely labelled nigrostriatal neurones. Brain Res 217: 245–263

    Google Scholar 

  • Somogyi P, Smith AD (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 Res 178: 3–15

    Google Scholar 

  • Somogyi P, Priestly JU, Cuello AC, Smith AD, Bolam JP (1982) Synaptic connection of substance P-immunoreactive nerve terminals in the substantia nigra of the rat. Cell Tissue Res 223: 469–486

    Google Scholar 

  • Staines WA, Nagy JI, Vincent S, Fibiger HC (1980) Neurotransmitters contained in the efferents of the striatum. Brain Res 194: 391–402

    Google Scholar 

  • Szabo J (1970) Projections from the body of the caudate nucleus in the rhesus monkey. Exp Neurol 27: 1–15

    Google Scholar 

  • Tachibana S, Araki I, Ohya S, Hoshida S (1982) Isolation and structure of dynorphin, an opioid peptide, from porcine duodenum. Nature 295: 339–340

    Google Scholar 

  • Tulloch IF, Arbuthnott GW, Wright AK (1978) Topographical organization of the striatonigral pathway revealed by anterograde and retrograde neuroanatomical tracing techniques. J Anat 127: 425–441

    Google Scholar 

  • Uhl GR, Goodman RR, Kuhar MJ, Childers SR, Snyder SH (1979) Immunohistochemical mapping of enkephalin containing cell bodies, fibers and nerve terminals in the brain stem of the rat. Brain Res 166: 75–94

    Google Scholar 

  • Ungerstedt U, Arbuthnott GW (1970) Quantitative recording of rotational behaviour in rats after 6-hydroxy-dopamine lesions of the nigrostriatal dopamine system. Brain Res 24: 485–493

    Article  CAS  PubMed  Google Scholar 

  • Ungerstedt U (1971a) Stereotaxic mapping of the monoamine pathway in the rat brain. Acta Physiol Scand Suppl 367: 1–48

    CAS  PubMed  Google Scholar 

  • Ungerstedt U (1971b) Postsynaptic supersensitivity after 6-hydroxy-dopamine induced degeneration of the nigro-striatal dopamine system. Acta Physiol Scand Suppl 367: 69–93

    CAS  PubMed  Google Scholar 

  • Ungerstedt U, Herrera-Marschitz M (1981) Behavioural pharmacology of dopamine receptor mechanisms. In: Stjärne L, Hedqvist P, Lagercrantz H, Wennmalm A (eds) Chemical neurotransmission: 75 years. Academic Press, New York, pp 481–494

    Google Scholar 

  • Ungerstedt U, Herrera-Marschitz M, Casas-Brugue M (1981) Are apomorphine, bromocriptine and the methylxanthines agonists at the same dopamine receptor. In: Gessa GL, Corsini GU (eds) Apomorphine and other dopaminomimetics, Vol 1. Basic pharmacology. Raven Press, New York, pp 85–93

    Google Scholar 

  • Vincent S, Hökfelt T, Christensson I, Terenius L (1982a) Immunohistochemical evidence for a dynorphin immunoreactive striato-nigral pathway. Eur J Pharmacol 85: 251–252

    Google Scholar 

  • Vincent SR, Hökfelt T, Christensson I, Terenius L (1982b) Dynorphin immunoreactive neurons in the central nervous system of the rat. Neurosci Lett 33: 185–190

    Google Scholar 

  • Wamsley JK, Young WS, Kuhar MJ (1980) Immunohistochemical localization of enkephalin in rat forebrain. Brain Res 190: 153–174

    Google Scholar 

  • Watson SJ, Khachaturian H, Akil H, Coy DH, Goldstein A (1982) Comparison of the distribution of dynorphin systems and enkephalin systems in brain. Science 218: 1134–1136

    Google Scholar 

  • Weber E, Roth KA, Barchas JD (1982) Immunohistochemical distribution of α-neo-endorphin/dynorphin neuronal systems in rat brain: evidence for colocalization. Proc Natl Acad Sci USA 79: 3062–3066

    Google Scholar 

  • Weber E, Barchas JD (1983) Immunohistochemical distribution of dynorphin B in rat brain: relation to dynorphin A and α-neoendorphin systems. Proc Natl Acad Sci USA 80: 1125–1129

    Google Scholar 

  • Williams RG, Dockray GJ (1983) Distribution of enkephalinrelated peptides in rat brain: immunohistochemical studies using antisera to Met-enkephalin and Met-enkephalin-Arg6- Phe7. Neuroscience 9: 563–586

    Google Scholar 

  • Williams MN, Faull RLM (1985) The striatonigral projection and nigrotectal neurons in the rat. A correlated light and electron microscopic study demonstrating a monosynaptic input to identified nigrotectal neurons using a combined degeneration and horseradish peroxidase procedure. Neuroscience 14: 991–1010

    Google Scholar 

  • Zamboni L, DeMartino C (1967) Buffered picric acid formaldehyde: a new rapid fixative for electron microscopy. J Cell Biol 148A: 35

    Google Scholar 

  • Zamir N, Palkovits M, Brownstein MJ (1983) Distribution of immunoreactive dynorphin in the central nervous system of the rat. Brain Res 280: 81–93

    Google Scholar 

  • Zamir N, Palkovits M, Weber E, Mezey E, Brownstein MJ (1984a) A dynorphinergic pathway of Leu-enkephalin production in substantia nigra. Nature 307: 643–645

    Google Scholar 

  • Zamir N, Palkovits M, Brownstein MJ (1984b) Distribution of immunoreactive dynorphin A1–8 in discrete nuclei of the rat brain: comparison with dynorphin A. Brain Res 307: 61–68

    Google Scholar 

  • Zamir N, Palkovits M, Brownstein MJ (1984c) Distribution of immunoreactive β-neo-endorphin in discrete areas of the rat brain and pituitary gland: comparison with α-neo-endorphin. J Neurosci 4: 1248–1252

    Google Scholar 

  • Zamir N, Palkovits M, Brownstein MJ (1984d) The distribution of immunoreactive α-neo-endorphin in the central nervous system of the rat. J Neurosci 4: 1240–1247

    Google Scholar 

  • Zamir N, Palkovits M, Weber E, Brownstein MJ (1984e) Distribution of immunoreactive dynorphin B in discrete areas of the rat brain and spinal cord. Brain Res 300: 121–127

    Google Scholar 

  • Zivkovic B, Oblin A, Barthohne G (1985) Progabide reverses the nigral substance P reduction induced by chronic impairments of dopaminergic transmission. Eur J Pharmacol 112: 253–255

    Google Scholar 

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Authors and Affiliations

  1. Department of Pharmacology, University of Uppsala, S-75124, Uppsala, Sweden

    I. Christensson-Nylander & L. Terenius

  2. Departments of Pharmacology, Karolinska Institutet, S-10401, Stockholm, Sweden

    M. Herrera-Marschitz & U. Ungerstedt

  3. Departments of Histology, Karolinska Institutet, S-10401, Stockholm, Sweden

    W. Staines & T. Hökfelt

  4. Department of Pharmacology and Therapeutics, McGill University, Montreal, Canada

    C. Cuello

  5. Department of Neurology, Technical University of München, D-8000, München, Federal Republic of Germany

    W. H. Oertel

  6. Department of Psychiatry, New York University, Medical Center, New York, NY, USA

    M. Goldstein

Authors
  1. I. Christensson-Nylander
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  2. M. Herrera-Marschitz
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  3. W. Staines
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  4. T. Hökfelt
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  5. L. Terenius
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  6. U. Ungerstedt
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  7. C. Cuello
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  8. W. H. Oertel
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  9. M. Goldstein
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Christensson-Nylander, I., Herrera-Marschitz, M., Staines, W. et al. Striato-nigral dynorphin and substance P pathways in the rat. Exp Brain Res 64, 169–192 (1986). https://doi.org/10.1007/BF00238213

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  • DOI: https://doi.org/10.1007/BF00238213

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