Advertisement

Multi-Collateralization of the Dopaminergic Nigrotectal Projection in the Rat

  • M. Takada
  • K. J. Campbell
  • T. Hattori
Part of the Advances in Behavioral Biology book series (ABBI, volume 39)

Abstract

In view of the existence of massive efferents projecting outside the basal ganglia, the substantia nigra (especially the pars reticulata (SNr)), in conjunction with the pallidum, has been recognized as an output source of the basal ganglia (Nauta, 1979). The superior colliculus (SC) (Hopkins and Niessen, 1976; Rinvik et al., 1976; Jayaraman et al., 1977; Deniau et al., 1978; Faull and Mehler, 1978; Graybiel, 1978; Beckstead et al., 1979) is one of two major target sites of the SNr (the other is the ventromedial thalamic nucleus (VM) (Rinvik, 1975; Carpenter et al., 1976; Clavier et al., 1976; Faull and Mehler, 1978; Beckstead et al., 1979)). The fiber projection from the SNr to the SC is relatively well-organized in a topographic manner; most of projection neurons originate in the ventral portion of the SNr through its rostral 2/3 extent, and terminate in the intermediate/deep layers of the SC through its caudal 2/3 extent. This nigrotectal pathway is predominantly ipsilateral and to a lesser degree contralateral (Hopkins and Niessen, 1976; Rinvik et al., 1976; Deniau et al., 1977; Jayaraman et al., 1977; Gerfen et al., 1982). The pathway has also been implicated in the initiation of saccadic eye movements (Wurtz and Goldberg, 1972; Stryker and Schiller, 1975; Graybiel, 1978; Schiller et al., 1980; Wurtz and Albano, 1980). Indeed, a subpopulation of SNr cells attenuate their activity prior to saccadic eye movements and exert a tonic, gamma-aminobutyric acid (GAGA)-ergic inhibition on saccade-related cells in the SC (Hikosaka and Wurtz, 1983, 1985a, b). Many clinical reports have shown that individuals suffering from parkinsonism often exhibit abnormal saccadic eye movements (De,Jong and Melvill-Jones, 1971; Melvill-Jones and DeJong, 1971; Corin et al., 1972; Shibasaki et al., 1979; Teräväinen and Calne, 1980; Shimizu et al., 1981; White et al., 1983). In this respect, we have recently suggested in the rat that a specific population of SNr cells may provide a critical neuronal substrate for such clinical findings (Takada et al., 1988a, b). Thus, this cell group, which is localized primarily in the ventrolateral portion of the SNr at its rostral level, projects to both the striatum and SC by way of axon collaterals (Takada et al., 1988a). At least part of these bifurcating projection neurons are dopaminergic and can be eliminated by injecting a parkinsonism-inducing drug, 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) into the medial forebrain bundle (MFB, nigrostriatal dopamine fiber tract) (Takada et al., 1988b).

Keywords

Substantia Nigra Superior Colliculus glutamiC Acid Decarboxylase Ipsilateral Striatum Medial Terminal Nucleus 
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., Domesick, V. B., and Nauta, W. J. H., 1979, Efferent connections of the substantia nigra and ventral tegmental area in the rat, Brain Res., 175: 191.PubMedCrossRefGoogle Scholar
  2. Bentivoglio, M., van der Kooy, D., and Kuypers, H. G. J. M., 1979, The organization of the efferent projections of the substantia nigra in the rat. A retrograde fluorescent double labeling study, Brain Res., 174: 1.Google Scholar
  3. Bizzi, E., 1968, Discharges of frontal eye field neurons during saccadic and following eye movements in unanesthetized monkeys, Exp. Brain Res., 6: 69.Google Scholar
  4. Carpenter, M. B., Nakano, K., and Kim, R., 1976, Nigrothalamic projections in the monkey demonstrated by autoradiographic technics, J. Comp. Neurol. 165: 401.Google Scholar
  5. Chevalier, G., Thierry, A. M., Shibazaki, T., and Féger, J., 1981, Evidence for a GABAergic inhibitory pathway in the rat, Neurosci. Lett. 21: 67.Google Scholar
  6. Clavier, R. M., Atmadja, S., and Fibiger, H. C., 1976, Nigrothalamic projections in the rat as demonstrated by orthograde and retrograde tracing techniques, Brain Res. Bull. 1: 379.Google Scholar
  7. Corin, M. S., Elizan, T. S., and Bender, M. B., 1972, Oculomotor function in patients with Parkinson’s disease, J. Neurol. Sci. 15: 251.Google Scholar
  8. DeJong, J. D., and Melvill-Jones, G., 1971, Akinesia, hypokinesia, and bradykinesia in the oculomotor system of patients with Parkinson’s disease Exp. Neurol. 32: 58.Google Scholar
  9. Deniau, J. M., Chevalier, G., and Figer, J., 1978, Electrophysiological study of the nigro-tectal pathway in the rat, Neurosci. Lett., 10: 215.Google Scholar
  10. Deniau, J. M., Hammond-LeGuyader, C., Féger, J., and McKenzie, J. S., 1977, Bilateral projection of nigro-collicular neurons: an electrophysiological analysis in the rat, Neurosci. Lett., 5: 45.Google Scholar
  11. Di Chiara, G., Porceddu, M. L., Morelli, M., Mulas, M. L., and Gessa, G. L., 1979, Evidence for a GABAergic projection from the substantia nigra to the ventromedial thalamus and to the superior colliculus of the rat, Brain Res., 176: 173.Google Scholar
  12. Faull, R L. M., and Mehler, W. R., 1978, The cells of origin of nigrotectal, ngrothalamic and nigrostriatal projections in the rat, Neuroscience 3: 989.PubMedCrossRefGoogle Scholar
  13. Faull, R L. M., Nauta, W. J. H., and Domesick, V. B., 1986, The visual cortico-striatonigral pathway in the rat, Neuroscience 19: 1119.PubMedCrossRefGoogle Scholar
  14. Gerten, C. R, Staines, W. A., Arbuthnott, G. W., and Fibiger, H. C., 1982, Crossed connections of the substantia nigra in the rat J. Comp. Neurol. 207: 283.Google Scholar
  15. Graybiel, A. M., 1978, Organization of the nigrotectal connection: an experimental tracer study in the cat. Brain Res., 143: 339.PubMedCrossRefGoogle Scholar
  16. Hikosaka, O., and Wurtz, R H., 1983, Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus, J. Neurophysiol. 49: 1285.Google Scholar
  17. Hikosaka, O., and Wurtz, R H., 1985a, Modification of saccadic eye movements by GABArelated substances. I. Effects of muscimol and bicucullin in monkey superior colliculus, J. Neurophysiol. 53: 266.Google Scholar
  18. Hikosaka, O., and Wurtz, R H., 1985b. Modification of saccadic eye movements by GABArelated substances. II. Effects of muscimol in monkey substantia nigra pars reticulata, J. Neurophysiol. 53: 292.Google Scholar
  19. Hopkins, D. A., and Niessen, L. W., 1976, Substantia nigra projections to the reticular formation, superior colliculus and central gray in the rat, cat and monkey. Neurosci. Lett. 2: 253.Google Scholar
  20. Jayaraman, A., Batton, R R, III, and Carpenter, M. B., 1977, Nigrotectal projections in the monkey: an autoradiographic study, Brain Res. 135: 147.PubMedCrossRefGoogle Scholar
  21. Kiinzle, H.. and Akert, K., 1977, Efferent connections of cortical area 8 (frontal eye field) in Macaca fascicularis. A reinvestigation using the autoradiographic technique, J. Comp. Neurol. 173: 147.Google Scholar
  22. Melis, R M., and Gale, K., 1983, Effects of dopamine agonists on gamma-aminobutyric acid (GABA) turnover in the superior colliculus: evidence that nigrotectal GABA projections are under the influence of dopaminergic transmission, J. Pharmacol. 226: 425.Google Scholar
  23. Melvill-Jones, G., and DeJong, J. D., 1971, Dynamic characteristics of saccadic eye movements in Parkinson’s disease, Exp. Neurol., 31: 17.Google Scholar
  24. Nauta, H. J. W., 1979, A proposed conceptual reorganization of the basal ganglia and telencephalon, Neuroscience 4: 1875.PubMedCrossRefGoogle Scholar
  25. Rinvik, E., 1975, Demonstration of nigrothalamic connections in the cat by retrograde axonal transport of horseradish peroxidase, Brain Res., 90: 313.PubMedCrossRefGoogle Scholar
  26. Rinvik, E., Grofova, I., and Ottersen, O. P., 1976, Demonstration of nigrotectal and nigroreticular projections in the cat by axonal transport of proteins, Brain Res. 112: 388.PubMedCrossRefGoogle Scholar
  27. Schiller, P. H., True, S. D., and Conway, J. L., 1980, Deficits in eye movements following frontal eye-field and superior colliculus ablations, J. Neurophysiol. 44: 1175.PubMedGoogle Scholar
  28. Shibasaki, H., Tsuji, S., and Kuroiwa, Y., 1979, Oculomotor abnormalities in Parkinson’s disease Archs Neurol., 36: 360.Google Scholar
  29. Shimizu, N., Naito, M., and Yoshida, M., 1981, Eye-head co-ordination in patients with Parkinsonism and cerebellar ataxia, J. Neurol. Neurosurg. Psychiat., 43: 509.Google Scholar
  30. Stryker, M. P., and Schiller, P. H., 1975, Eye and head movements evoked by electrical stimulation of monkey superior colliculus, Exp. Brain Res., 23: 103.Google Scholar
  31. Takada, M., Li, Z. K., and Hattori, T., 1987, A note on the projections of pars compacta neurons within pars reticulata of the substantia nigra in the rat Brain Res. Bull., 18: 285.Google Scholar
  32. Takada, M., Li, Z. K., and Hattori, T., 1988a, Collateral projection from the substantia nigra to the striatum and superior colliculus in the rat, Neuroscience, 25: 563.PubMedCrossRefGoogle Scholar
  33. Takada, M., Li, Z. K., and Hattori, T., 1988b, Dopaminergic nigrotectal projection in therat, Brain Res., 457: 165.PubMedCrossRefGoogle Scholar
  34. Teräväinen, H., and Calne, D. B., 1980, Studies of parkinsonian movement: I. Programming and execution of eye movements, Acta Neurol. Scand. 62:137.Google Scholar
  35. Vincent, S. R., Hattori, T., and McGeer, E. G., 1978, The nigrotectal projection: a biochemical and ultrastructural characterization, Brain Res., 151: 159.PubMedCrossRefGoogle Scholar
  36. White, O. B., Saint-Cyr, J. A., Tomlinson, R. D., and Sharpe, J. A., 1983, Ocular motor deficits in Parkinson’s disease. II. Control of the saccadic and smooth pursuit systems, Brain. 106: 571.Google Scholar
  37. Wurtz, R H., and Albano, J. E., 1980, Visual-motor function of the primate superior colliculus, Ann. Rev. Neurosci. 3: 189.Google Scholar
  38. Wurtz, R. H., and Goldberg. M. E., 1972, Activity of superior colliculus in behaving monkey. III. Cells discharging before eye movements, J. Neurophysiol., 35: 575.Google Scholar

Copyright information

© Plenum Press, New York 1991

Authors and Affiliations

  • M. Takada
    • 1
  • K. J. Campbell
    • 1
  • T. Hattori
    • 1
  1. 1.Department of AnatomyUniversity of TorontoTorontoCanada

Personalised recommendations