Functional Architecture of the Rodent Substantia Nigra Pars Reticulata: Evidence for Segregated Channels

  • Jean-Michel Deniau
  • Gilles Chevalier
Part of the Advances in Behavioral Biology book series (ABBI, volume 41)


While it is widely accepted that basal ganglia are involved in motor processes, the precise role of this system in motor functions is still unclear. Since the basal ganglia receive afferents from all the major functional sectors of the cortical mantle, it has been suggested that they constitute a suitable system to integrate motivation, cognition and perception for the elaboration of movement. A pertinent question however is to know exactly how the various cortical products are processed by the basal ganglia. Until recent past years, current views on the functional organization of basal ganglia were strongly influenced by their apparent funnel-like structure. Due to the reduction in nuclear volume along the cortico-striato-nigral and striato-pallidal circuits, the basal ganglia were regarded as an integrative device where the multiple cortical processings are compiled for the elaboration of a motor act. However, cumulative evidences in primate for a parallel arrangement of the transbasal ganglia pathways has led to the idea that basal ganglia maintain rather than mingle the functional heterogeneity of the cortical mantle (Alexander et al., 1986; Alexander and Crutcher, 1990). It is in fact well documented, in a variety of mammalian species, that the cortical functional mosaic is orderly mapped onto the striatal nuclear complex. While the sensorimotor cortices innervate predominantly the putamen (Kunzle, 1977; Flaherty and Graybiel, 1991), the associative frontal, parietal and temporal areas project mostly to the caudate (Goldman and Nauta, 1977; Yeterian and Pandya, 1991) and the allocortex to the accumbens (McGeorge and Faull, 1989; Berendse et al., 1992).


Basal Ganglion Superior Colliculus Thalamic Nucleus Parallel Arrangement Cortical Mantle 
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  1. Alexander, G. E., and Crutcher, M.D., 1990, Functional architecture of basal ganglia circuits:neural substrates of parallel processing, Trends Neurosci. 13:266–271.PubMedCrossRefGoogle Scholar
  2. Alexander, G.E., DeLong, M.R., and Strick, P.L., 1986, Parallel organization of functionally segregated circuits linking basal ganglia and cortex, Ann. Rev. Neurosci. 9:357–381.PubMedCrossRefGoogle Scholar
  3. Beckstead, R.M., and Frankfurter, A., 1982, The distribution and some morphological features of substantia nigra and ventral tegmental area in the rat, Neuroscience 7:2377–2388.PubMedCrossRefGoogle Scholar
  4. Berendse, H.W., Galis de Graaf, Y., and Groenewegen, HJ., 1992, Topographical organisation and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat, J. Comp. Neurol.316:314–347.PubMedCrossRefGoogle Scholar
  5. Bickford, M. E., and Hall, W. C., 1989, Collateral projections of predorsal bundle cells of the superior colliculus in the rat, J. Comp. Neurol. 283:86–106.PubMedCrossRefGoogle Scholar
  6. Chevalier, G., and Deniau, J. M., 1984, Spatio-temporal organization of a branched tecto-spinal/tecto diencephalic neuronal system, Neuroscience 12:427–439.PubMedCrossRefGoogle Scholar
  7. Chevalier, G., and Deniau J.M., 1990, Disinhibition as a basic process in the expression of striatal functions, Trends Neurosci. 13:277–280.PubMedCrossRefGoogle Scholar
  8. Deniau, J.M., and Chevalier, G., 1992, The lamellar organization of the rat substantia nigra pars reticulata:distribution of projection neurons, Neuroscience 46:361–377.PubMedCrossRefGoogle Scholar
  9. Domesick, V.B., 1977, The topographical organization of the striatonigral connection in the rat, A nat. Rec. 187:567.Google Scholar
  10. Faull, R.L.M., and Mehler, W.R., 1978, The cells of origin of nigrotectal, nigrothalamic and nigrostriatal projection in the rat, Neuroscience 3:989–1002.PubMedCrossRefGoogle Scholar
  11. Flaherty, A.W., and Graybiel, A.M., 1991, Corticostriatal transformations in the primate somatosensory system. Projections from physiologically mapped body part representations, J. Neurophysiol. 66:1249–1263.PubMedGoogle Scholar
  12. François, C, Percheron, G., and Yelnik, J., 1984, Localization of nigrostriatal, nigrothalamic and nigrotectal neurons in ventricular coordinates in macaques, Neuroscience 13:61–76.PubMedCrossRefGoogle Scholar
  13. Gerfen, C.R., 1985, The neostriatal mosaic. I Compartmental organization of projections from the neostriatum to the substantia nigra in the rat, J. Comp. Neurol. 236:454–476.PubMedCrossRefGoogle Scholar
  14. Goldman, P.S., and Nauta, W.J.H. 1977, An intricately patterned prefrontocaudate projection in the rhesus monkey, J. Comp. Neurol. 171:369–386.CrossRefGoogle Scholar
  15. Ilinsky, I. A., Jouandet, M. L., and Golanan-Rakic P. S., 1985, Organization of the nigrothalamocortical system in the rhesus monkey, J. Comp. Neurol. 236:315–330.PubMedCrossRefGoogle Scholar
  16. Jimenez-Castellanos, J., and Reinoso-Suarez, F., 1985, Topographical organization of the afferent connections of the principal ventromedial thalamic nucleus in the cat, J. Comp. Neurol. 236:297–314.PubMedCrossRefGoogle Scholar
  17. Kunzle, H., 1977, Projections from primary somatosensory cortex to basal ganglia and thalamus in the monkey, Exp. Brain Res.30:481–492.PubMedCrossRefGoogle Scholar
  18. McGeorge, A.J., and Faull, R.L.M., 1989, The organization of the projection from the cerebral cortex to the striatum in the rat, Neuroscience 29:503–537.PubMedCrossRefGoogle Scholar
  19. Nauta, W.J.H., Smith, G.P., Faull, R.L.M., and Domesick, V.B. 1978, Efferent connections and nigral afferents of the nucleus accumbens septi in the rat, Neuroscience 3:385–401.PubMedCrossRefGoogle Scholar
  20. Redgrave, P., Odenkule, A., and Dean, P., 1986, Tectal cells of origin of the predorsal bundle in rat:location and segregation from ipsilateral descending pathway, Exp. Brain Res. 63:279–293.PubMedCrossRefGoogle Scholar
  21. Smith, Y., and Parent, A., 1986, Differential connections of caudate nucleus and putamen in the squirrel monkey (Saimiri sciureus), Neuroscience 18:347–371.PubMedCrossRefGoogle Scholar
  22. Sahibzada, N., Dean, P., and Redgrave, P., 1986, Movements resembling orientation and avoidance elicited by electrical stimulation of the superior colliculus in rats, J. Neurosci. 6:723–733.PubMedGoogle Scholar
  23. Westby, G.W.M., Keay, K.A., Re. Jgrave, P., Dean, P., and Bannister M., 1990 Output pathways from the rat superior colliculus mediating approach and avoidance have different sensory properties, Exp.Brain. Res. 81:626–638.PubMedCrossRefGoogle Scholar
  24. Wilson, C. J., and Phelan, K. D., 1982, Dual topographic representation of neostriatum in the globus pallidus of rats, Brain Res. 243:354–359.PubMedCrossRefGoogle Scholar
  25. Yeterian, E.H., and Pandya, D.N., 1991, Prefirontostriatal connections in relation to cortical architectonic organization in rhesus monkeys, J. Comp. Neurol. 312:43–67.PubMedCrossRefGoogle Scholar
  26. Yeterian, E. H., and Van Hoesen, G. W., 1978, Cortico-striate projections in the rhesus monkey:the organization of certain cortico-caudate connections, Brain Res. 139:43–63.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1994

Authors and Affiliations

  • Jean-Michel Deniau
    • 1
  • Gilles Chevalier
    • 1
  1. 1.Laboratoire des Communications et Régulations Cellulaires, URA 1199Université Pierre et Marie CurieParisFrance

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