Skip to main content
SpringerLink
Log in

Dopaminergic neurotransmission in somatodendritic and terminal areas of the rat brain: susceptibility to modulation by D 1 and D2 receptors and to axotomy

  • Full Papers
  • Published:
Journal of Neural Transmission / General Section JNT Aims and scope Submit manuscript

Summary

We have investigated the influence of D1 and D2 dopamine receptor active drugs on dopamine (DA) release in substantia nigra (SN), striatum and limbic forebrain in intact and in hemisected rats in vivo. DA release was indirectly assessed as 3-methoxytyramine (3-MT) accumulation following monoamine oxidase inhibition by pargyline. Hemisection per se had no effect on the 3-MT accumulation in the SN. Neither, had SCH 23390, SK & F28393, or cisflupentixol any effect in the SN in intact animals or in the lesioned side in hemisected animals. SCH 23390 slightly increased the 3-MT accumulation both in the striatum and limbic forebrain, indicating a stimulatory action on DA release, but SK & F38393 had no effect in these brain regions. A difference between the striatum and the limbic forebrain was that the effects of SCH 23390, and cis-FPX were almost abolished following hemisection in the limbic fore-brain, but only partially reduced in the striatum. In summary, our data give further support for the concept that neither D 1 nor D 2 dopamine receptors have any pronounced influence on the DA release in the SN. The data also indicate operational differences in the feedback regulation of limbic versus striatal dopaminergic transmission.

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

  • Andén N-E (1977) Shortlasting increase in the synthesis and utilization of noradrenaline due to axotomy-induced irritation. Acta Physiol Scand 100: 51–55

    Google Scholar 

  • Andén N-E (1980) Regulation of monoamine synthesis and utilization by receptors. In: Szekeres L (ed) Handbook of experimental pharmacology, vol 27. Springer, Berlin Heidelberg New York, pp 429–462

    Google Scholar 

  • Andén N-E, Golembiowska-Nikitin K, Thronström U (1982) Selective stimulation of DA and noradrenaline autoreceptors by B-HT 920 and B-HT 933, respectively. Naunyn-Schmiedebergs Arch Pharmacol 321: 100–104

    Google Scholar 

  • Anton AH, Sayre DF (1962) A study of the factors affecting the aluminum oxidetrihy-droxyindole procedure for the analysis of catecholamines. J Pharmacol Exp Ther 138: 360–375

    Google Scholar 

  • Arnt J, Hyttel J (1985) Different involvement of dopamine D-1 and D-2 receptors in the circling behaviour induced by apomorphine, SK & F38393, pergolide and LY 171555 in 6-hydroxydopamine-lesioned rats. Psychopharmacology 85: 346–352

    Google Scholar 

  • Bannon MJ, Reinhard JF, Bunnex EB, Roth RH (1982) Unique response to antipsychotic drugs due to absence of terminal autoreceptors in mesocortical DA neurones. Nature 296: 444–446

    Google Scholar 

  • Bischoff S, Heinrich M, Sonntag JM, Krauss J (1986) The D-1 dopamine receptor antagonist SCH 23390 also interacts potently with brain serotonin (5-HT2) receptors. Eur J Pharmacol 129: 367–370

    Google Scholar 

  • Bouthenet M-L, Martres M-P, Sales N, Schwartz J-C (1987) A detailed mapping of dopamine D-2 receptors in rat central nervous system by autoradiography with [125I]iodosulpiride. Neuroscience 20: 117–155

    Google Scholar 

  • Brown EE, Damsma G, Cumming P, Fibiger HC (1991) Interstitial 3-methoxytyramine reflects striatal dopamine release: an in vivo microdialysis study. J Neurochem 57: 701–707

    Google Scholar 

  • Carlson JH, Bergstrom DA, Walters JR (1986) Neurophysiological evidence that D-1 dopamine receptors blockade attenuates postsynaptic but not autoreceptor-mediated effects of dopamine agonists. Eur J Pharmacol 23: 237–251

    Google Scholar 

  • Carlsson A, Lindqvist M (1973) Effect of ethanol on the hydroxylation of tyrosine and tryptophan in rat brain in vivo. J Pharm Pharmacol 25: 437–440

    Google Scholar 

  • Chéramy A, Barbeito L, Godeheu G, Desce JM, Pittaluga A, Galli T, Artaud F, Glowinski J (1990) Respective contributions of neuronal activity and presynaptic mechanisms in the control of the in vivo release of dopamine. J Neural Transm 29: 183–193

    Google Scholar 

  • Cross AJ, Mashal RD, Johnson JA, Owen F (1983) Preferential inhibition of ligand binding to calf striatal dopamine D 1 receptors by SCH 23390. Neuropharmacology 22: 1327–1329

    Google Scholar 

  • Cuello AC, Iversen LL (1978) Interaction of dopamine with other neurotransmitters in the rat substantia nigra: a possible functional role of dendritic dopamine. In: Garattini S, Pujol JF, Samanin R (eds) Interactions between putative neurotransmitters in the brain. Raven Press, New York, pp 127–149

    Google Scholar 

  • Di Chiara G, Imperato A (1985) Rapid tolerance to neuroleptic-induced stimulation of dopamine release in freely moving rats. J Pharmacol Exp Ther 235: 487–494

    Google Scholar 

  • Felice LJ, Felice JD, Kissinger PT (1978) Determination of catechol-amines in rat brain parts by reverse-phase ion-pair liquid chromatography. J Neurochem 31: 1461–1465

    Google Scholar 

  • Filloux FM, Wamsley JK, Dawson TM (1987) Presynaptic and postsynaptic D 1 dopamine receptors in the nigrostriatal system of the rat brain: a quantitative autoradiographic study using the selective D 1 antagnoist [3H]SCH 23390. Brain Res 408: 205–209

    Google Scholar 

  • Gale K, Guidotti A, Costa E (1977) Dopamine sensitive adenylate cyclase: location in substantia nigra. Science 195: 503–505

    Google Scholar 

  • Hassler R, Back IJ (1969) Unbalanced rations of striatal dopamine and serotonin after experimental interruption of strionigral connections in rat. In: Gillingham FJ, Donaldson IML (eds) Third symposium on Parkinson's disease. Livingstone, Edinburgh London, pp 29–37

    Google Scholar 

  • Hjorth S, Carlsson A (1988) In vivo receptor binding, neurochemical and functional studies with the dopamine D-1 receptor antagonist SCH 23390. J Neural Transm 72: 83–97

    Google Scholar 

  • Imperato A, Mulas A, Di Chiara G (1987) The D-1 antagonist SCH 23390 stimulates while the D-1 agonist SK & F 38393 fails to affect dopamine release in the dorsal caudate of freely moving rats. Eur J Pharmacol 142: 177–181

    Google Scholar 

  • Jaskiw GE, Weinberger DR, Crawley JN (1991) Microinjection of apomorphine into the prefrontal cortex of the rat reduces dopamine metabolite concentrations in microdialysate from the caudate nucleus. Biol Psychiatry 29: 703–706

    Google Scholar 

  • Kehr W (1976) 3-Methoxytyramine as an indicator of impulse-induced dopamine release in rat brain in vivo. Naunyn-Schmiedebergs Arch Pharmacol 293: 209–215

    Google Scholar 

  • Kelland MD, Freeman AS, Chiodo LA (1988) SKF 38392 alters the rate dependent D 2-mediated inhibition of nigrostriatal but not mesoaccumbens dopamine neurons. Synapse 2: 416–423

    Google Scholar 

  • Leviel V, Kerny C, Barberis C, Guibert B, Daudet F (1984) Blockade by frontocortical lesion of reciprocal regulation between the two nigrostriatal dopaminergic pathways. Neuroscience 13: 53–59

    Google Scholar 

  • Magnusson O, Nilsson LB, Westerlund D (1980) Simultaneous determination of dopamine, DOPAC and homovanillic acid. Direct injection of supernatants from brain tissue homogenates in a liquid chromotography-electrochemical detection system. J Chromatogr 221: 237–247

    Google Scholar 

  • Mailman RB, Schultz DW, Lewis MH, Staples L, Rollema H, Dehaven DL (1984) SCH 23390: a selective dopamine antagonist with potent D 2 behavioral actions. Eur J Pharmacol 101: 159–160

    Google Scholar 

  • Markwell MAK, Haas SM, Bieber LL, Tolbert NE (1978) A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem 87: 206–210

    Google Scholar 

  • Morelli M, Carboni E, Devoto S, Di Chiara G (1987) 6-Hydroxydopamine lesions reduce specific [3H]sulpiride binding in the rat substantia nigra: direct evidence for the existence of nigral D-2 autoreceptors. Eur J Pharmacol 140: 99–104

    Google Scholar 

  • Nieoullon A, Chéramy A, Glowinski J (1977) Release of dopamine in vivo from cat substantia nigra. Nature 266: 375–377

    Google Scholar 

  • Nissbrandt H, Sundström E, Johnsson G, Hjorth S, Carlsson A (1989) Synthesis and release of dopamine in rat brain: comparison between substantia nigra pars compacta, pars reticulata and striatum. J Neurochem 52: 1170–1182

    Google Scholar 

  • Onali P, Mereu G, Olianas MC, Bunse B, Rossetti Z, Gessa GL (1985) SCH 23390, a selective D 1 dopamine receptor blocker, enhances the firing rate of nigral dopaminergic neurons but fails to activate striatal tyrosine hydroxylase. Brain Res 340: 1–7

    Google Scholar 

  • Phillipson OT, Emson PC, Horn AS, Jessel T (1977) Evidence concerning the anatomical location of the dopamine stimulated adenylate cyclase in the substantia nigra. Brain Res 136: 45–58

    Google Scholar 

  • Plantjé JF, Daus FJ, Hansen HA, Stoof JC (1984) SCH 23390 blocks D-1 and D-2 dopamine receptors in rat neostriatum in vitro. Naunyn-Schmiedebergs Arch Pharmacol 327: 180–182

    Google Scholar 

  • Porceddu ML, Giorgi O, De Montis G, Mele S, Cocco L, Ongini E, Biggio G (1987) 6-Hydroxydopamine-induced degeneration of nigral dopamine neurons: differential effect on nigral and striatal D-1 dopamine receptors. Life Sci 41: 697–706

    Google Scholar 

  • Robertson GS, Damsma G, Fibiger HC (1991) Characterization of dopamine release in the substantia nigra by in vivo microdialysis in freely moving rats. J Neurosci 11: 2209–2216

    Google Scholar 

  • Romo R, Chéramy A, Godeheu G, Glowinski J (1984) Direct commissural pathways are involved in the enhanced releas of dopamine induced in the contralateral caudate nucleus and substantia nigra by unilateral application of GABA in the cat thalamic motor nuclei. Brain Res 308: 43–52

    Google Scholar 

  • Saller CF, Salama AI (1986) 3-Methoxytyramine accumulation: effects of typical neuro-leptics and various atypical compounds. Naunyn-Schmiedebergs Arch Pharmacol 334: 125–132

    Google Scholar 

  • Santiago W, Westerink BHC (1991) Characterization and pharmacological responsiveness of dopamine release recorded by microdialysis in the substantia nigra of conscious rats. J Neurochem 57: 738–747

    Google Scholar 

  • Savasta M, Dubois A, Benavides J, Scatton B (1986) Different neuronal location of [3H]SCH 23390 binding sites in pars reticulata and pars compacta of the substantia nigra in the rat. Neurosci Lett 72: 265–271

    Google Scholar 

  • Starr MS (1987) Opposing roles of dopamine D1 and D2 receptors in nigra γ-[3 H]aminobutyric acid release? J Neurochem 49: 1042–1049

    Google Scholar 

  • Svensson K, Hjorth S, Clark D, Carlsson A, Wikström A, Andersson B, Sanchez D, Johansson AM, Arvidsson L-E, Hacksell U, Nilsson JLG (1986) (+)-UH 232 and (+)-UH 242: novel stereoselective dopamine receptor antagonists with preferential action on autoreceptors. J Neural Transm 65: 1–27

    Google Scholar 

  • Westerink BHC (1979) Effects of drugs on the formation of 3-methoxy-tyramine, a dopamine metabolite, in the substantia nigra, striatum, nucleus accumbens and tuberculum olfactorium of the rat. J Pharm Pharmacol 31: 94–99

    Google Scholar 

  • Wood PL, Altar CA (1988) Dopamine release in vivo from nigrostriatal, mesolimbic, and mesocortical neurons: utility of 3-methoxytyramine measurements. Pharmacol Rev 40: 163–187

    Google Scholar 

  • Zetterström T, Ungerstedt U (1984) Effects of apomorphine on the in vivo release of dopamine and its metabolites, studied by brain dialysis. Eur J Pharmacol 97: 29–34

    Google Scholar 

Download references

Author information

Author notes

  1. H. Nissbrandt

    Present address: Department of Pharmacology, University of Göteborg, Sweden

Authors and Affiliations

  1. Department of Pharmacology, University of Göteborg, Sweden

    S. Hjorth

Authors
  1. H. Nissbrandt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Hjorth
    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

Nissbrandt, H., Hjorth, S. Dopaminergic neurotransmission in somatodendritic and terminal areas of the rat brain: susceptibility to modulation by D 1 and D2 receptors and to axotomy. J. Neural Transmission 90, 13–26 (1992). https://doi.org/10.1007/BF01250514

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01250514

Keywords

Search

Navigation