Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1992 Dec 1;89(23):11214–11218. doi: 10.1073/pnas.89.23.11214

Distinct presynaptic control of dopamine release in striosomal- and matrix-enriched areas of the rat striatum by selective agonists of NK1, NK2, and NK3 tachykinin receptors.

L Tremblay 1, M L Kemel 1, M Desban 1, C Gauchy 1, J Glowinski 1
PMCID: PMC50520  PMID: 1280822

Abstract

Using a sensitive in vitro microperfusion method, the effects of selective and potent agonists of NK1, NK2, and NK3 tachykinin receptors ([Pro9]SP, ([Lys5,MeLeu9,Nle10]NKA-(4-10), and [Pro7]NKB, respectively) on the presynaptic control of dopamine release were investigated in striosomal-enriched (area rich in [3H]naloxone binding sites) and matrix-enriched areas of the rat striatum. Marked differences could be demonstrated as follows: (i) when used at 0.1 microM, the NK1 agonist stimulated the release of [3H]dopamine continuously synthesized from [3H]tyrosine in both compartments, while the NK2 and NK3 agonists enhanced the release of [3H]dopamine only in the matrix; (ii) the stimulatory effect of the NK3 agonist was less pronounced than those of the NK1 and NK2 agonists; (iii) the NK1 agonist-evoked responses were tetrodotoxin (1 microM) sensitive, while those of the NK2 and NK3 agonists were, respectively, partially and totally tetrodotoxin resistant; (iv) specific receptors are involved in these responses since the stimulatory effects of the NK1 and NK2 agonists were, respectively, blocked by potent antagonists of NK1 (RP-67580; 1 microM) and NK2 (SR-48968; 1 microM) receptors, while these antagonists did not affect the NK3 agonist-evoked response; (v) the indirect stimulatory effect of the NK1 agonist was partially reduced under local blockade of cholinergic transmission in the matrix but not in the striosomal-enriched area. Interestingly, this study also revealed mismatches between autoradiographic data and receptor-mediated responses, since NK2 binding sites could not be observed in the striatum while NK3 but not NK1 binding sites were visualized in the striosomal-enriched area.

Full text

PDF
11214

Images in this article

11215Image
on p.11215
11216Image
on p.11216
11217Image
on p.11217

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arai H., Emson P. C. Regional distribution of neuropeptide K and other tachykinins (neurokinin A, neurokinin B and substance P) in rat central nervous system. Brain Res. 1986 Dec 10;399(2):240–249. doi: 10.1016/0006-8993(86)91514-3. [DOI] [PubMed] [Google Scholar]
  2. Baruch P., Artaud F., Godeheu G., Barbeito L., Glowinski J., Chéramy A. Substance P and neurokinin A regulate by different mechanisms dopamine release from dendrites and nerve terminals of the nigrostriatal dopaminergic neurons. Neuroscience. 1988 Jun;25(3):889–898. doi: 10.1016/0306-4522(88)90042-5. [DOI] [PubMed] [Google Scholar]
  3. Besson M. J., Graybiel A. M., Quinn B. Co-expression of neuropeptides in the cat's striatum: an immunohistochemical study of substance P, dynorphin B and enkephalin. Neuroscience. 1990;39(1):33–58. doi: 10.1016/0306-4522(90)90220-x. [DOI] [PubMed] [Google Scholar]
  4. Burgunder J. M., Young W. S., 3rd Distribution, projection and dopaminergic regulation of the neurokinin B mRNA-containing neurons of the rat caudate-putamen. Neuroscience. 1989;32(2):323–335. doi: 10.1016/0306-4522(89)90081-x. [DOI] [PubMed] [Google Scholar]
  5. Chassaing G., Lavielle S., Loeuillet D., Robilliard P., Carruette A., Garret C., Beaujouan J. C., Saffroy M., Petitet F., Torrens Y. Selective agonists of NK-2 binding sites highly active on rat portal vein (NK-3 bioassay). Neuropeptides. 1991 Jun;19(2):91–95. doi: 10.1016/0143-4179(91)90137-8. [DOI] [PubMed] [Google Scholar]
  6. Chesselet M. F., Robbins E. Regional differences in substance P-like immunoreactivity in the striatum correlate with levels of pre-protachykinin mRNA. Neurosci Lett. 1989 Jan 2;96(1):47–53. doi: 10.1016/0304-3940(89)90241-3. [DOI] [PubMed] [Google Scholar]
  7. Desban M., Gauchy C., Kemel M. L., Besson M. J., Glowinski J. Three-dimensional organization of the striosomal compartment and patchy distribution of striatonigral projections in the matrix of the cat caudate nucleus. Neuroscience. 1989;29(3):551–566. doi: 10.1016/0306-4522(89)90130-9. [DOI] [PubMed] [Google Scholar]
  8. Elliott P. J., Iversen S. D. Behavioural effects of tachykinins and related peptides. Brain Res. 1986 Aug 27;381(1):68–76. doi: 10.1016/0006-8993(86)90691-8. [DOI] [PubMed] [Google Scholar]
  9. Garret C., Carruette A., Fardin V., Moussaoui S., Peyronel J. F., Blanchard J. C., Laduron P. M. Pharmacological properties of a potent and selective nonpeptide substance P antagonist. Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10208–10212. doi: 10.1073/pnas.88.22.10208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gerfen C. R., Baimbridge K. G., Miller J. J. The neostriatal mosaic: compartmental distribution of calcium-binding protein and parvalbumin in the basal ganglia of the rat and monkey. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8780–8784. doi: 10.1073/pnas.82.24.8780. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gerfen C. R., Herkenham M., Thibault J. The neostriatal mosaic: II. Patch- and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems. J Neurosci. 1987 Dec;7(12):3915–3934. doi: 10.1523/JNEUROSCI.07-12-03915.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gerfen C. R. Substance P (neurokinin-1) receptor mRNA is selectively expressed in cholinergic neurons in the striatum and basal forebrain. Brain Res. 1991 Aug 9;556(1):165–170. doi: 10.1016/0006-8993(91)90563-b. [DOI] [PubMed] [Google Scholar]
  13. Gerfen C. R. The neostriatal mosaic: multiple levels of compartmental organization. Trends Neurosci. 1992 Apr;15(4):133–139. doi: 10.1016/0166-2236(92)90355-c. [DOI] [PubMed] [Google Scholar]
  14. Gerfen C. R., Young W. S., 3rd Distribution of striatonigral and striatopallidal peptidergic neurons in both patch and matrix compartments: an in situ hybridization histochemistry and fluorescent retrograde tracing study. Brain Res. 1988 Sep 13;460(1):161–167. doi: 10.1016/0006-8993(88)91217-6. [DOI] [PubMed] [Google Scholar]
  15. Graybiel A. M., Baughman R. W., Eckenstein F. Cholinergic neuropil of the striatum observes striosomal boundaries. Nature. 1986 Oct 16;323(6089):625–627. doi: 10.1038/323625a0. [DOI] [PubMed] [Google Scholar]
  16. Graybiel A. M. Neurotransmitters and neuromodulators in the basal ganglia. Trends Neurosci. 1990 Jul;13(7):244–254. doi: 10.1016/0166-2236(90)90104-i. [DOI] [PubMed] [Google Scholar]
  17. Graybiel A. M., Ragsdale C. W., Jr Histochemically distinct compartments in the striatum of human, monkeys, and cat demonstrated by acetylthiocholinesterase staining. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5723–5726. doi: 10.1073/pnas.75.11.5723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Herkenham M. Mismatches between neurotransmitter and receptor localizations in brain: observations and implications. Neuroscience. 1987 Oct;23(1):1–38. doi: 10.1016/0306-4522(87)90268-5. [DOI] [PubMed] [Google Scholar]
  19. Herkenham M., Pert C. B. Mosaic distribution of opiate receptors, parafascicular projections and acetylcholinesterase in rat striatum. Nature. 1981 Jun 4;291(5814):415–418. doi: 10.1038/291415a0. [DOI] [PubMed] [Google Scholar]
  20. Innis R. B., Andrade R., Aghajanian G. K. Substance K excites dopaminergic and non-dopaminergic neurons in rat substantia nigra. Brain Res. 1985 Jun 3;335(2):381–383. doi: 10.1016/0006-8993(85)90499-8. [DOI] [PubMed] [Google Scholar]
  21. Jimenez-Castellanos J., Graybiel A. M. Subdivisions of the dopamine-containing A8-A9-A10 complex identified by their differential mesostriatal innervation of striosomes and extrastriosomal matrix. Neuroscience. 1987 Oct;23(1):223–242. doi: 10.1016/0306-4522(87)90285-5. [DOI] [PubMed] [Google Scholar]
  22. Jiménez-Castellanos J., Graybiel A. M. Compartmental origins of striatal efferent projections in the cat. Neuroscience. 1989;32(2):297–321. doi: 10.1016/0306-4522(89)90080-8. [DOI] [PubMed] [Google Scholar]
  23. Kanazawa I., Ogawa T., Kimura S., Munekata E. Regional distribution of substance P, neurokinin alpha and neurokinin beta in rat central nervous system. Neurosci Res. 1984 Dec;2(1-2):111–120. doi: 10.1016/0168-0102(84)90009-9. [DOI] [PubMed] [Google Scholar]
  24. Kemel M. L., Desban M., Glowinski J., Gauchy C. Distinct presynaptic control of dopamine release in striosomal and matrix areas of the cat caudate nucleus. Proc Natl Acad Sci U S A. 1989 Nov;86(22):9006–9010. doi: 10.1073/pnas.86.22.9006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Krause J. E., Chirgwin J. M., Carter M. S., Xu Z. S., Hershey A. D. Three rat preprotachykinin mRNAs encode the neuropeptides substance P and neurokinin A. Proc Natl Acad Sci U S A. 1987 Feb;84(3):881–885. doi: 10.1073/pnas.84.3.881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Krebs M. O., Trovero F., Desban M., Gauchy C., Glowinski J., Kemel M. L. Distinct presynaptic regulation of dopamine release through NMDA receptors in striosome- and matrix-enriched areas of the rat striatum. J Neurosci. 1991 May;11(5):1256–1262. doi: 10.1523/JNEUROSCI.11-05-01256.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nakanishi S. Mammalian tachykinin receptors. Annu Rev Neurosci. 1991;14:123–136. doi: 10.1146/annurev.ne.14.030191.001011. [DOI] [PubMed] [Google Scholar]
  28. Petit F., Glowinski J. Stimulatory effect of substance P on the spontaneous release of newly synthesized [3H]dopamine from rat striatal slices: a tetrodotoxin-sensitive process. Neuropharmacology. 1986 Sep;25(9):1015–1021. doi: 10.1016/0028-3908(86)90196-6. [DOI] [PubMed] [Google Scholar]
  29. Petitet F., Glowinski J., Beaujouan J. C. Evoked release of acetylcholine in the rat striatum by stimulation of tachykinin NK-1 receptors. Eur J Pharmacol. 1991 Jan 3;192(1):203–204. doi: 10.1016/0014-2999(91)90095-8. [DOI] [PubMed] [Google Scholar]
  30. Reid M. S., Herrera-Marschitz M., Ungerstedt U. Effects of intranigral substance P and neurokinin A on striatal dopamine release--II. Interactions with bicuculline and naloxone. Neuroscience. 1990;36(3):659–667. doi: 10.1016/0306-4522(90)90008-r. [DOI] [PubMed] [Google Scholar]
  31. Saffroy M., Beaujouan J. C., Torrens Y., Besseyre J., Bergström L., Glowinski J. Localization of tachykinin binding sites (NK1, NK2, NK3 ligands) in the rat brain. Peptides. 1988 Mar-Apr;9(2):227–241. doi: 10.1016/0196-9781(88)90255-0. [DOI] [PubMed] [Google Scholar]
  32. Stoessl A. J., Szczutkowski E., Glenn B., Watson I. Behavioural effects of selective tachykinin agonists in midbrain dopamine regions. Brain Res. 1991 Nov 29;565(2):254–262. doi: 10.1016/0006-8993(91)91657-m. [DOI] [PubMed] [Google Scholar]
  33. Trovero F., Herve D., Desban M., Glowinski J., Tassin J. P. Striatal opiate mu-receptors are not located on dopamine nerve endings in the rat. Neuroscience. 1990;39(2):313–321. doi: 10.1016/0306-4522(90)90270-e. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES