Advertisement

The Development of Striatal Compartments: From Proliferation to Patches

  • Derek van der Kooy
  • Gord Fishell
  • Leslie A. Krushel
  • Janice G. Johnston
Part of the Advances in Behavioral Biology book series (ABBI, volume 32)

Abstract

The conception of the organization of the striatum has changed in recent times from that of a homogeneous structure to that of a distinctly compartmentalized one. Part of this change is really a question of level of analysis. On a single cell level, morphological studies have demonstrated that the vast majority of striatal cells are of a single medium spiny type (Kemp and Powell, 1971). On a multicellular level, the striatum can be divided into two compartments, the patch and the matrix, which can be differentiated on the basis of several neurochemical and hodological markers. In single striatal sections, the small patches appear imbedded into the larger matrix compartment, but it is clear from serial section reconstructions that the patches form a continuous labyrinthian compartment through the striatum (Graybiel and Ragsdale, 1978). The distribution of the patches can be delineated in the adult by high levels of opiate receptors (Kent et al., 1982; Pert et al., 1976), substance P (Gerfen, 1984; Haber and Watson, 1985), neurotensin (Goedart et al., 1984), and afferents from the prefrontal cortex (Donoghue and Herkenham, 1986, Gerfen, 1984). In complementary fashion, the matrix compartment can be identified in the adult by high levels of somatostatin (Gerfen, 1984), neurotensin receptors (Goedart et el., 1984), acetylcholinesterase (Graybiel, 1984), thalamic terminals from the centromedian parafasicular complex (Herkenham and Pert, 1981), and terminations from neurons located in sensorimotor cortex (Donoghue and Herkenham, 1986).

Keywords

Ventricular Zone Opiate Receptor Striatal Cell Patch Cell Matrix Compartment 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Angevine, J.B. and Sidman, R.L. Autoradiographic study of cell migration during histogenesis of cerebral cortex in mice Nature (London), 192 (1961) 766–768.CrossRefGoogle Scholar
  2. Arbuthnott, G. and Wright, A.K., 1982, Some non-fluorescent connections of the nigro-neostriatal dopamine neurones, Brain Research Bulletin, 9:367–378.PubMedCrossRefGoogle Scholar
  3. Beach, T.G. and McGeer, E.G., 1984 The distribution of substance P in the primate basal ganglia: an immunohistochemical study of baboon and human brain, Neurosci., 13: 29–52.CrossRefGoogle Scholar
  4. Brand, S. and Rakic, P, 1979, Genesis of the primate neostriatum [3H]thymidine autonradiograpic analysis of the time of neuron origin in the rhesus monkey. Neuroscience, 4: 767–778.PubMedCrossRefGoogle Scholar
  5. Butcher, L.L. and Hodge, G.K., 1976, Postnatal development of acetylcholinesterase in the caudate putament and substantia nigra of rats, Brain Research, 106: 223–240.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. of Neuroscience, in press.Google Scholar
  7. Floeter, M.K. and Jones, E.G., 1985a, The morphology and phased outgrowth of callosal axons in the fetal rat, Dev. Brain Research, 22: 7–18.CrossRefGoogle Scholar
  8. Floeter, M.K. and Jones, E.G., 1985b, Transplantation of fetal postmitotic neurons to rat cortex: survival, early pathway choices and long-term projections of outgrowing axons, Developmental Brain Research, 22: 19–38.CrossRefGoogle Scholar
  9. Gerfen, C.R., 1984, The neostriatal mosaic: compartmentalization of corticostriatal input and striatonigral output systems, Nature, 311: 461– 464.PubMedCrossRefGoogle Scholar
  10. Goedart, M., Mantyh, P.W., Emson, P.C. and Hunt, S.P., 1984, Inverse relationship between neurotensin receptors and neurotensin-like immunoreactivity in cat striatum, Nature307: 543–546.CrossRefGoogle Scholar
  11. Goldman-Rakic, P.S., 1982, Cytoarchitectonic heterogeneity of the primate neostriatum: subdivision into island and matrix cellular compartments. J. Comp. Neurol., 205: 398–413.PubMedCrossRefGoogle 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., Pickel, V.M., Joh, T., Reis, D.J., and Ragsdale, C.W., 1978, Direct demonstration of a correspondence between the dopamine islands and acetylicholinesterase patches in the developing striatum, Proc. Natl. Acad. Sci. USA., 75: 5871–5875.CrossRefGoogle Scholar
  14. Graybiel, A.M., Ragsdale, C.W., Yoneoka, E.S. and Elde, R.P., 1981, An immunohistochemical study of enkephalins and other neuropeptides in the striatum of the cat with evidence that the opiate peptides are arranged to form mosaic patterns in register with the striosomal compartments visible by acetylcholinesterase staining, Neuroscience, 6: 377–397.PubMedCrossRefGoogle Scholar
  15. Haber, S.N. and Watson, J., 1985, The comparative distribution of enkephalin, dynorphin and substance P in the human globus pallidus and basal forebrain, Neuroscience, 14: 1011–1024.PubMedCrossRefGoogle Scholar
  16. Harding, K., Rushlow, C., Doyle, H.J., Hoey, T., and Levine, M., 1986, Cross regulatory interactions among pair-rule genes in Drosphilia, Science, 233: 953–954.PubMedCrossRefGoogle Scholar
  17. Herkenham, M. and Pert, C.B., 1981, Mosaic distribution of opiate receptors, parafasicular projections and acetylcholinesterase in the rat striatum, Nature, 291: 415–418.PubMedCrossRefGoogle Scholar
  18. Johnston, J.G., Boyd, S.R. and van der Kooy, D., 1987, Compartmentaliza-tion of the embryonic striatum after intraocular transplantation, Dev. Brain Research, submitted.Google Scholar
  19. Kemp, J.M. and Powell, T.P.S., 1971, The structure of the caudate nucleus of the cat: light and electron microscopy, Phil. Trans. B, 262: 383– 401.Google Scholar
  20. Kent, J.T., Pert, C.B., and Herkenham, M., 1982, Ontogeny of opiate receptors in rat forebrain: visualization by in vitro autoradiography, Dev, Brain, Research., 2: 487–504.CrossRefGoogle Scholar
  21. Kolb, B, Whishaw, I.Q., and van der Kooy, D., 1986, Brain development in the neonatally decorticated rat, Brain Research, 397: 315–326PubMedCrossRefGoogle Scholar
  22. Krushel, L.A., Connolly, J.A., and van der Kooy, D., 1986, In vitro reassociation of neurons from the patch component of the rat striatum, Soc. Neurosci. Abtr., 12: 866.Google Scholar
  23. Lanca, A.J., Boyd, S., Kolb, B.E., and van der Kooy, 1986, The development of a patchy organization of the rat striatum, Dev. Brain Research, 27: 1–10.CrossRefGoogle Scholar
  24. Levine, J.M., Beasley, L., and Stallcup, U.B., 1984, The D 1,1 antigen: a cell surface marker for germinal cells of the central nervous system, J. Neurosci., 4: 820–831.PubMedGoogle Scholar
  25. Levitt, P., Cooper, M.L., and Rakic, P., 1981, Coexistence of neuronal and glial precursor cells in the cerebral ventricular zone of the fetal monkey: an ultrastructural immunoperoxidase analysis, J. Neurosci., 1: 27–39.PubMedGoogle Scholar
  26. Marchand, R. and Lajoie, L., 1986, Histogenesis of the striopallidal system in the rat. Neurogenesis of its neurons, Neurosci., 17: 573–590.CrossRefGoogle Scholar
  27. Moon, S.L., 1984, Prenatal haloperidol alters striatal dopamine and opiate receptors, Brain Research, 323: 109–113.PubMedCrossRefGoogle Scholar
  28. Moon Edley, S., and Herkenham, M., 1984, Comparative development of striatal opiate receptors in the developing striatum, Brain Research, 305: 27–42.PubMedCrossRefGoogle Scholar
  29. Murrin, L.C., and Ferrier, J.R., 1984, Ontogeny of the rat striatum: correspondence of dopamine terminals, opiate receptors and acetylcholinesterase, Neurosci. Lett., 47: 155–160.PubMedCrossRefGoogle Scholar
  30. Nagy, J.I., Carter, D.A., and Fibiger, H., 1978, Anterior striatal projections to the globis pallidus, ontopeduncular nucleus and substantia nigra in the rat: the GABA connection, Brain Research, 158: 15– 29.PubMedCrossRefGoogle Scholar
  31. Newman-Gage, H., and Graybiel, A.M., 1986, Synapse-related antibody immunostaining in the developing cat striatum: a light and electron microscopic study, Soc. Neurosci. Abstr., 12: 1326Google Scholar
  32. Olson, L, and Seiger, A., 1972, Early ontogeny of central monomine neurons in the rat: fluorescence histochemical observations. Z. Anat. Entwickl.-Gesch., 138: 301–316.CrossRefGoogle Scholar
  33. Olson, L., and Seiger, A., and Fuxe, 1972, Heterogeneity of striatal and limbic dopamine innervation: highly fluorescent islands in developing and adult rats, Brain Research, 44: 283–288.PubMedCrossRefGoogle Scholar
  34. Olson, L., Vanderhaegen, J.J., Freedman, R., Henschen S., Hoffer, B., and Seiger, A., 1985, Combined grafts of ventral tegmental area and nucleus accumbens in oculo. Histochemical and electrophysiological characterization, Exp. Brain Research, 59: 325–337.Google Scholar
  35. Pert, C.B., Kuhar, M.J., and Synder, S.H., 1976, Opiate receptors: autoradiographic localization in rat brain, Proc. Nat. Acad. Sci. USA, 73: 3729–3733.PubMedCrossRefGoogle Scholar
  36. Rakic, P., 1975, Timing of major ontogenetic events in the visual cortex of the rhesus monkey, N.A. Buchwald and M.A.B. Brazier, eds., in: “Brain Mechanisms in Mental Retardation”, Academic Press, New York, pp. 3– 40.Google Scholar
  37. Russchen, F.T., 1987, On the organization of the basal ganglia of a reptile, in: “Basal Ganglia — Structure and Function II”, M.B. Carpenter and R. Jayaraman, eds., Plenum Press, New York, pg.-261.Google Scholar
  38. Specht, L.A., Pickel, V.M., Joh, T.H., and Reis, D.J., 1981, Light microscopic immunocytochemical localization of tyrosine hydorxylase in prenatal rat brain, II. Late ontogeny, J. Comp. Neurol. 199: 255–276.PubMedCrossRefGoogle Scholar
  39. van der Kooy, D., 1984, Developmental relationships between opiate receptors and dopamine in the formation of caudate/putamen patches, Dev. Brain Research, 14: 300–303.CrossRefGoogle Scholar
  40. van der Kooy, D., and Fishell, G., 1986, Neuronal birthdate underlies the development of striatal compartments in the brain, Brain Research, in press.Google Scholar
  41. Waechter, R.V. and Jaensch, B., 1972, Generation times of the matrix cells during embryonic brain development: an autoradiographic study in rats, Brain Research, 46: 235–250.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1987

Authors and Affiliations

  • Derek van der Kooy
    • 1
  • Gord Fishell
    • 1
  • Leslie A. Krushel
    • 1
  • Janice G. Johnston
    • 1
  1. 1.Department of AnatomyUniversity of TorontoTorontoCanada

Personalised recommendations