Advertisement

The Neostriatal Mosaic: Compartmental Organization of Mesostriatal Systems

  • Charles R. Gerfen
Part of the Advances in Behavioral Biology book series (ABBI, volume 32)

Abstract

The compartmental organization of the dopaminergic and nondopaminergic containing projections from the midbrain to the striatum was examined in the rat. In order to determine the relative inputs from various midbrain neurons to either of the striatal “patch” or “matrix” compartments methods were combined to label mesostriatal afferents with the anterograde axonal tracer PHA-L and to compare their distribution relative to autoradiographically localized mu-opiate receptors in patches. A non-dopaminergic nigrostriatal projection was identified to the striatal matrix compartment. Two dopaminergic (DA) mesostriatal systems were identified. One system, directed to the striatal matrix compartment, was shown to arise from neurons in the ventral tegmental area (A10 DA cell group), the dorsal tier of the substantia nigra pars compacta (dorsal A9 DA cell group) and the retrorubral area (A8 DA cell group). The other system, directed to the striatal patch compartment, was shown to arise from neurons in the ventral tier of the substantia nigra pars compacta (ventral A9 DA cell group) and from DA cells in the substantia nigra pars reticulata. The asynchronous development of the “patch” and “matrix” mesostriatal systems provides a means of further characterization. Injections of the neurotoxin 6-hydroxydopamine into the striatum on the day of birth (P0), when the patch system is in place but prior to the ingrowth of the matrix dopaminergic system, resulted in the select and long-lasting depletion of the patch dopaminergic system. Such lesions provided a clear delineation of dopaminergic neurons projecting to the striatal matrix, as they were selectively spared by the neonatal lesions. First, the distribution of these neurons matched that deduced from the PHA-L tracing studies. Second, the dendrites of matrix directed neurons are distributed amongst other DA neurons, whereas those DA neurons which project to the patches possess dendrites which are distributed into the non-dopaminergic parts of the substantia nigra pars reticulata. Third, a brain calcium binding protein (calbindin D28kD or CaBP) is expressed by those dopaminergic neurons which project to the striatal matrix and not by those which project to the patches.

Keywords

Tyrosine Hydroxylase Substantia Nigra Dopaminergic Neuron Ventral Tegmental Area Nigrostriatal System 
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. Beckstead, R.M. (1984) Complementary mosaic distributions of thalamic and nigral axons in the caudate nucleus of the cat: double anterograde labeling combining autoradiography and wheat germ-HRP histochemistry. Brain Res. 335: 153–159.CrossRefGoogle Scholar
  2. Bjorklund, A. and O. Lindvall (1975) Dopamine in dendrites of substantia nigra neurons: suggestions for a role in dendritic terminals. Brain Res. 83: 531–537.PubMedCrossRefGoogle Scholar
  3. Cheramy, A., V. Leviel and J. Glowinski (1981) Dendritic release of dopamine in the substantia nigra. Nature 289: 537–542.PubMedCrossRefGoogle Scholar
  4. Chiodo, L.A., and B.S. Bunney (1983) Typical and atypical neuroleptics: differential effects of chronic administration on the activity of A9 and A10 midbrain dopaminergic neruons. J. Neurosci. 3: 1607–1619.PubMedGoogle Scholar
  5. Creese, I. (1983) Classical and atypical antipsychotic drugs: new insights. TINS 6: 479–481.Google Scholar
  6. Dahlstrom, A., and K. Fuxe (1964) Evidence for the existence of monoamine-containing neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brain stem neruons. Acta Physiol. Scand. suppl. 232: 62: 1–31.Google Scholar
  7. Donoghue, J.P. and M. Herkenham (1986) Neostriatal projections from individual cortical fields conform to histochemically distinct striatal compartments in the rat. Brain Res. 365: 397–403.PubMedCrossRefGoogle Scholar
  8. Fallon, J.H. and R.Y. Moore (1978) Catecholamine innervation of the basal forebrain. IV. Topography of the dopamine projection to the basal forebrain and neostriatum. J. Comp. Neurol. 180: 545–580.PubMedCrossRefGoogle Scholar
  9. Fibiger, H.C. and A.G. Phillips (1986) Reward, motivation, cognition: psychobiology of mesotelencephalic dopamine systems. In: Handbook of Physiology, The Nervous System Vol. IV: Intrinsic Regulatory Systems of the Brain. (F.E. Bloom, ed.) American Physiological Society, Baltimore, pp: 647–675.Google Scholar
  10. Gerfen, C.R. (1984) The neostriatal mosaic: compartmentalization of corticostriatal input and striatonigral output systems. Nature 311: 461– 464.PubMedCrossRefGoogle Scholar
  11. Gerfen, C.R. (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.PubMedCrossRefGoogle Scholar
  12. Gerfen, C.R., K.G. Baimbridge and J.J. Miller (1985) The neostriatal mosaic: Compartmental distribution of calcium binding protein and parvalbumin in the basal ganglia of the rat and monkey. Proc. Natl. Acad. Sci. (USA) 82: 8780–8784.CrossRefGoogle Scholar
  13. Gerfen, C.R. and P.E. Sawchenko (1984) An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons and terminals: Immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris- leucoagglutinin (PHA-L). Brain Res. 290: 219–238.PubMedCrossRefGoogle Scholar
  14. Gerfen, C.R. and P.E. Sawchenko (1985) A method for anterograde axonal tracing of chemically specified circuits in the central nervous system: combined Phaseolus vulgaris- leucoagglutinin (PHA-L) tract tracing and immunohistochemistry. Brain Res. 343: 144–150.PubMedCrossRefGoogle Scholar
  15. 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
  16. Graybiel, A.M. and C.W. Ragsdale, Jr. (1978) Histochemically distinct compartments in the striatum of human,monkey and cat demonstrated by acetylcholinesterase staining. Proc. Natl. Acad. Sci. USA 75: 5723–5726.PubMedCrossRefGoogle Scholar
  17. Groves, P.M., C.J. Wilson, S.J. Young and G.V. Rebec (1975) Selfinhimbition by dopaminergic neurons. Science 190: 522–529.PubMedCrossRefGoogle Scholar
  18. Heimer, L. and R.D. Wilson (1975) The subcortical projections to the allocortex: similarities in the neural associations of the hippocampus, the piriform cortex and the neocortex. In: Golgi Centennial Symposium (ed. M. Santini) pp 177–193, Raven Press, New York.Google Scholar
  19. Herkenham, M., S. Moon Edley and J. Stuart (1984) Cell clusters in the nucleus accumbens of the rat, and the mosaic relationship of opiate receptors, acetylcholinesterase and subcortical afferent terminations. Neuroscience [11: 561–593.PubMedCrossRefGoogle Scholar
  20. Herkenham, M. and C.B. Pert (1981) Mosaic distribution of opiate receptors, parafascicular projections and acetylcholinesterase in rat striatum. Nature (London) 291: 415–418.CrossRefGoogle Scholar
  21. Herkenham, M. and C.B. Pert (1982) Light microscopic localization of brain opiate receptors: a general autoradiographic method which preserves tissue quality. J. Neurosci. 2: 1129–1149.PubMedGoogle Scholar
  22. Hornykiewicz (1966) Dopamine (3-hydroxytryptamine) and brain function. Pharmacol. Rev. 18: 925–964.PubMedGoogle Scholar
  23. Kelley, A.E., V.B. Domesick and W.J.H. Nauta (1982) The amygdalostriatal projection in the rat- an anatomical study by anterograde and retrograde tracing methods. Neuroscience 7: 615–630.PubMedCrossRefGoogle Scholar
  24. Lindvall, O., A. Bjorklund, R.Y. Moore and U. Stenevi (1974) Mesencephalic dopamine neurons projecting to neocortex. Brain Res. 81: 325–331.PubMedCrossRefGoogle Scholar
  25. Lindvall, O., A. Bjorklund and I. Divac (1978) Organization of catecholamine neurons projecting to the frontal cortex in the rat. Brain Res. 142:1–24.PubMedCrossRefGoogle Scholar
  26. Nauta, W.J.H., G.P. Smith, R.L.M. Faull and V.B. Domesick (1978) Efferent connections and nigral afférents of the nucleus accumbens septi in the rat. Neuroscience 3: 385–401.PubMedCrossRefGoogle Scholar
  27. Olson, L., A. Seiger and K. Fuxe (1972) Heterogeneity of striatal and limbic dopamine innervation: highly fluorescent islands in developing and adult rats. Brain Res. 44: 283–288.PubMedCrossRefGoogle Scholar
  28. Pert, C.B., M.J.Kuhar and S.H. Snyder (1976) Opiate receptor: autoradiographic localization in rat brain. Proc. Natl. Acad. Sci. USA 73: 3729–3733.PubMedCrossRefGoogle Scholar
  29. Ragsdale, C.W., Jr. and A.M. Graybiel (1981) The fronto-striatal projection in the cat and monkey and its relationship to inhomogeneities established by acetylcholinesterase histochemistry. Brain Res. 208: 259– 266.PubMedCrossRefGoogle Scholar
  30. Shepard, P.D. and D.C. German (1987a) Regional differences in substantia nigra neurons: electrophysiological properties. Neuroscience, in press.Google Scholar
  31. Shepard, P.D. and D.C. German (1987b) Regional differences in substantia nigra dopamine neurons: pharmacological properties. Neruoscience, in press.Google Scholar
  32. Swanson, L.W. (1982) The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res. Bull. 9: 321–353.PubMedCrossRefGoogle Scholar
  33. Ungerstedt, U. (1971) Stereotaxic mapping of monoamine pathways in the rat brain. Acta Physiol. Scand. suppl. 367: 1–48.Google Scholar
  34. White, F.J. and R.Y. Wang (1983) Differential effects of classical and atypical antipsychotic drugs on A9 and A10 dopamine neurons. Science 221 : 1054–1057.PubMedCrossRefGoogle Scholar
  35. Wright, A.K. and G.W. Arbuthnott (1981) The pattern of innervation of the corpus striatum by the substantia nigra. Neuroscience 6: 2063–2067.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1987

Authors and Affiliations

  • Charles R. Gerfen
    • 1
  1. 1.Laboratory of Cell BiologyNIMHBethesdaUSA

Personalised recommendations