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Patchy Distribution of Substance P Receptor Immunoreactivity in Developing Rat Striatum

  • Masahiko Takada
  • Hironobu Tokuno
  • Takeshi Kaneko
  • Ryuichi Shigemoto
  • Noboru Mizuno
Part of the Advances in Behavioral Biology book series (ABBI, volume 47)

Abstract

It is the general view that substance P (SP) innervation of the striatum is provided primarily by local axon collaterals of SP-containing striatal neurons which send their axons preferentially to the internal pallidal segment and the substantia nigra pars reticulata (Gerfen, 1992; Graybiel, 1990; Wilson, 1990). Accumulated evidence indicates that the main targets of such intrinsic SP-containing fibers are composed of two subsets of striatal interneurons: large aspiny cholinergic neurons and medium-sized aspiny somatostatin-containing ones (Aubry et al., 1993; Kaneko et al., 1993; Martone et al., 1992; Gerfen, 1991; Elde et al., 1990; Bolam et al., 1986). In particular, our recent studies have clearly demonstrated that the postsynaptic expression of SP receptor (SPR) immunoreactivity in the adult striatum is localized to these interneurons, and that the dendritic network of the SPR-immunoreactive interneurons extends homogeneously over the striatum (Nakaya et al., 1994; Kaneko et al., 1993; Shigemoto et al., 1993). On the other hand, SP-binding sites in the developing striatum have previously been reported to be distributed transiently in a patchy fashion (Quirion and Dam, 1986). In this context, it is of interest to look into the developmental changeover of intrastriatal distribution of SPR immunoreactivity. Here, we asked three major questions as to (1) whether striatal SPR immunoreactivity is distributed in a patchy fashion during development; if so, (2) whether the SPR-immunoreactive patches are in register with the striatal patch or matrix compartment; and (3) whether SPR immunoreactivity within the SPR-immunoreactive patches is located in striatal interneurons.

Keywords

Cholinergic Neuron Receptor Immunoreactivity Striatal Projection Neuron Matrix Compartment Striatal Interneuron 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Aubry, J.-M., Schulz, M.-F., Pagliusi, S., Schulz, P., and Kiss, J.Z., 1993, Coexpression of dopamine D2 and substance P (neurokinin-1) receptor messenger RNAs by a subpopulation of cholinergic neurons in the rat striatum, Neuroscience 53: 417–424.PubMedCrossRefGoogle Scholar
  2. Bolam, J.P., and Izzo, P.N., 1988, 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.PubMedCrossRefGoogle Scholar
  3. Bolam, J.P., Ingham, C.A., Izzo, P.N., Levey, A.I., Rye, D.B., Smith, A.D., and Wainer, B.H., 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.PubMedCrossRefGoogle Scholar
  4. Elde, R., Schalling, M., Ceccatelli, S., Nakanishi, S., and Hökfelt, T., 1990, Localization of neuropeptide receptor mRNA in rat brain: Initial observations using probes for neurotensin and substance P receptors, Neurosci. Lett. 120: 134–138.PubMedCrossRefGoogle Scholar
  5. Fentress, J.C., Stanfield, B.B., and Cowan, W.M., 1981, Observations on the development of the striatum in mice and rats, Anat. Embryol. 163: 275–298.PubMedCrossRefGoogle Scholar
  6. Fishell, G., and van der Kooy, D., 1987, Pattern formation in the striatum: Developmental changes in the distribution of striatonigral neurons, J. Neurosci. 7: 1969–1978.PubMedGoogle Scholar
  7. Fishell, G., and van der Kooy, D., 1989, Pattern formation in the striatum: Developmental changes in the distribution of striatonigral projections, Dev. Brain Res. 45: 239–255.CrossRefGoogle Scholar
  8. Fishell, G., and van der Kooy, D., 1991, Pattern formation in the striatum: Neurons with early projections to the substantia nigra survive the cell death period, J. Comp. Neurol. 312: 33–42.PubMedCrossRefGoogle Scholar
  9. Gerfen, C.R., 1991, Substance P (neurokinin-1) receptor mRNA is selectively expressed in cholinergic neurons in the striatum and basal forebrain, Brain Res. 556: 165–170.PubMedCrossRefGoogle Scholar
  10. Gerfen, C.R., 1992, The neostriatal mosaic: Multiple levels of compartmental organization in the basal ganglia, Annu. Rev. Neurosci. 15: 285–320.PubMedCrossRefGoogle Scholar
  11. Gerfen, C.R., Baimbridge, K.G., and Thibault, J., 1987, The neostriatal mosaic: III. Biochemical and developmental dissociation of patch-matrix mesostriatal systems, J. Neurosci. 7: 3935–3944.PubMedGoogle Scholar
  12. Graybiel, A.M., 1984, Correspondence between the dopamine islands and striosomes of the mammalian striatum, Neuroscience 13: 1157–1187.PubMedCrossRefGoogle Scholar
  13. Graybiel, A.M., 1990, Neurotransmitters and neuromodulators in the basal ganglia, Trends Neurosci. 13: 244–254.PubMedCrossRefGoogle Scholar
  14. Kaneko, T., Shigemoto, R., Nakanishi, S., and Mizuno, N., 1993, Substance P receptor-immunoreactive neurons in the rat neostriatum are segregated into somatostatinergic and cholinergic aspiny neurons, Brain Res. 631:297–303.PubMedCrossRefGoogle Scholar
  15. Liu, F.-C., and Graybiel, A.M., 1992, Heterogeneous development of calbindin-D28K expression in the striatal matrix, J. Comp. Neurol. 320: 304–322.PubMedCrossRefGoogle Scholar
  16. Martone, M.E., Armstrong, D.M., Young, S.J., and Groves, P.M., 1992, Ultrastructural examination of enkephalin and substance P input to cholinergic neurons within the rat neostriatum, Brain Res. 594: 253–262.PubMedCrossRefGoogle Scholar
  17. Nakaya, Y., Kaneko, T., Shigemoto, R., Nakanishi, S., and Mizuno, N., 1994, Immunohistochemical localization of substance P receptor in the central nervous system of the adult rat, J. Comp. Neurol. 347: 249–274.PubMedCrossRefGoogle Scholar
  18. Quirion, R., and Dam, T.-V, 1986, Ontogeny of substance P receptor binding sites in rat brain, J. Neurosci. 6: 2187–2199.PubMedGoogle Scholar
  19. Shigemoto, R., Nakaya, Y., Nomura, S., Ogawa-Meguro, R., Ohishi, H., Kaneko, T., Nakanishi, S., and Mizuno, N., 1993, Immunocytochemical localization of rat substance P receptor in the striatum, Neurosci. Lett. 153: 157–160.PubMedCrossRefGoogle Scholar
  20. Snyder-Keller, A.M., 1991, Development of striatal compartmentalization following pre-or postnatal dopamine depletion, J. Neurosci. 11:810–821.PubMedGoogle Scholar
  21. van der Kooy, D., and Fishell, G., 1987, Neuronal birthdate underlies the development of striatal compartments, Brain Res. 401: 155–161.PubMedCrossRefGoogle Scholar
  22. Wilson, C.J., 1990, Basal ganglia, in: The Synaptic Organization of the Brain, 3rd ed. (G.M. Shepherd, ed.), Oxford University Press, New York, pp. 279–316.Google Scholar
  23. Zahm, D.S., Eggerman, K.W., Sprung, R.F., Wesche, D.E., and Payne, E., 1990, Postnatal development of striatal neurotensin immunoreactivity in relation to clusters of substance P immunoreactive neurons and the “dopamine islands” in the rat, J. Comp. Neurol. 296: 403–414.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1996

Authors and Affiliations

  • Masahiko Takada
    • 1
  • Hironobu Tokuno
    • 1
  • Takeshi Kaneko
    • 1
  • Ryuichi Shigemoto
    • 1
  • Noboru Mizuno
    • 1
  1. 1.Department of Morphological Brain Science, Faculty of MedicineKyoto UniversityKyoto 606-01Japan

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