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The total number, time of origin and kinetics of proliferation of neurons comprising the deep cerebellar nuclei in the rhesus monkey

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Summary

The genesis of the neurons that form the cerebellar nuclei was studied by autoradiographic methods in 30 postnatal rhesus monkeys which were exposed to 3H-thymidine at various embryonic (E) and postnatal (P) ages. As a basis for this quantitative analysis, five 2–3 month old monkeys were used for cell counting and estimation of the total number of neurons in each of the cerebellar nuclei. The results show that the cerebellar nuclei on each side contain 131,000 neurons. There are 68,000 neurons in the dentate nucleus, 25,000 neurons in the posterior interposed nucleus, and 19,000 neurons in both the anterior interposed and fastigial nuclei. All of the neurons comprising the deep nuclei are generated during the first half of the 165 day gestation period in this species. Although neurogenesis lasts from E30 through E70, approximately 81% of the neuron population is generated during a one week period between E36 and E40, with the peak of proliferation occurring at E36. Before E45 both large (maximum diameter greater than 35 μm) and small (maximum diameter 35 μm or less) neurons are produced simultaneously; after this period only small neurons are generated. Although no clearcut spatio-temporal gradients of neurogenesis could be discerned along any of the cardinal axes, each cerebellar nucleus has a somewhat distinctive developmental history in terms of the onset and cessation of neurogenesis and the tempo of cell proliferation. Thus, genesis of neurons destined for the dentate nucleus begins earlier and ends later than proliferation of the neurons that ultimately comprise the fastigial nucleus. Generation of the neurons destined for the anterior and posterior interposed nuclei follows an intermediate time course. The present data on neurogenetic sequences in the deep nuclei could not be correlated with the zonal pattern of reciprocal axonal connections that link the deep nuclei and overlying cerebellar cortex.

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References

  • Altman J (1969) Autoradiographic and histological studies of postnatal neurogenesis. III. Dating the time of production and onset of differentiation of cerebellar microneurons in rats. J Comp Neurol 136: 269–294

    Google Scholar 

  • Altman J, Bayer SA (1978) Prenatal development of the cerebellar system in the rat. I. Cytogenesis and histogenesis of the deep nuclei and the cortex of the cerebellum. J Comp Neurol 179: 23–48

    Google Scholar 

  • Angevine JB, Jr (1970) Time of neuron origin in the diencephalon of the mouse. An autoradiographic study. J Comp Neurol 139: 129–188

    PubMed  Google Scholar 

  • Brand S, Rakic P (1979) Genesis of primate neostriatum: [3H] thymidine autoradiographic analysis of the time of origin in the rhesus monkey. Neuroscience 4: 767–778

    Google Scholar 

  • Brodal A, Pompeiano O (1957) The vestibular nuclei in the cat. J Anat (Lond) 91: 438–454

    Google Scholar 

  • Cammermeyer J (1967) Artifactual displacement of neuronal nucleoli in paraffin sections. J Hirnforsch 9: 209–224

    Google Scholar 

  • Chan-Palay V (1977) Cerebellar dentate nucleus: Organization, cytology, and transmitters. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Chan-Palay V, Palay SL, Wu J-Y (1979) Gamma-aminobutyric acid pathways in the cerebellum studied by retrograde and anterograde transport of glutamic acid decarboxylase antibody after in vivo injections. Anat Embryol 157: 1–14

    Google Scholar 

  • Courville J, Cooper CW (1970) The cerebellar nuclei of Macaca mulatta: a morphological study. J Comp Neurol 140: 241–254

    Google Scholar 

  • Dietrichs E, Walberg F (1979) The cerebellar corticonuclear and nucleocortical projections in the cat as studied with anterograde and retrograde transport of horseradish peroxidase. I. The paramedian lobule. Anat Embryol 158: 13–19

    Google Scholar 

  • Gould BB (1979) The organization of afferents to the cerebellar cortex in the cat: Projections from the deep cerebellar nuclei. J Comp Neurol 184: 27–42

    Google Scholar 

  • Gould BB, Graybiel AM (1976) Afferents to the cerebellar cortex in the cat: evidence for an intrinsic pathway leading from the deep nuclei to the cortex. Brain Res 110: 601–611

    Google Scholar 

  • Haines DE, Pearson JC (1979) Cerebellar corticonuclear-nucleocortical topography: a study of the tree shrew (Tupaia) paraflocculus. J Comp Neurol 187: 745–758

    Google Scholar 

  • Konigsmark BW (1970) Methods for counting of neurons. In: Nauta WJH, Ebbeson SOE (eds) Contemporary research methods in neuroanatomy. Springer, Berlin Heidelberg New York, pp 315–340

    Google Scholar 

  • Kornguth SE, Anderson JW, Scott G (1968) The development of synaptic contacts in the cerebellum of Macaca mulatta. J Comp Neurol 132: 531–546

    Google Scholar 

  • Lange W (1978) The myelination of the cerebellar cortex in the cat. Cell Tissue Res 188: 509–520

    Google Scholar 

  • Larsell O, Jansen J (1972) The comparative anatomy and histology of the cerebellum: The human cerebellum, cerebellar connections, and cerebellar cortex. University of Minnesota Press, Minneapolis

    Google Scholar 

  • McCrea RA, Bishop GA, Kitai ST (1978) Morphological and electrophysiological characteristics of projection neurons in the nucleus interpositus of the cat cerebellum. J Comp Neurol 181: 397–420

    Google Scholar 

  • Miale IL, Sidman RL (1961) An autoradiographic analysis of histogenesis in the mouse cerebellum. Exp Neurol 4: 277–296

    Google Scholar 

  • Rakic P (1973) Kinetics of proliferation and latency between final cell division and onset of differentiation of cerebellar stellate and basket neurons. J Comp Neurol 147: 523–546

    Google Scholar 

  • Rakic P (1976) Local circuit neurons. MIT Press, Cambridge

    Google Scholar 

  • Rakic P (1977) Genesis of the dorsal lateral geniculate nucleus in the rhesus monkey: site and time of origin, kinetics of proliferation, routes of migration and pattern of distribution of neurons. J Comp Neurol 176: 23–52

    Google Scholar 

  • Rakic P, Sidman RL (1968) Subcommissural organ and adjacent ependyma: autoradiographic study of their origin in the mouse brain. Am J Anat 122: 317–336

    Google Scholar 

  • Rakic P, Sidman RL (1970) Histogenesis of cortical layers in human cerebellum, particularly the lamina dissecans. J Comp Neurol 139: 473–500

    Google Scholar 

  • Sidman RL (1970) Autoradiographic methods and principles for study of the nervous system with thymidine-H3. In: Nauta WJH, Ebbeson SOE (eds) Contemporary research methods in neuroanatomy. Springer, Berlin Heidelberg New York, pp 252–274

    Google Scholar 

  • Stanton GB (1980) Afferents to oculomotor nuclei from area “y” in Macaca mulatta. An anterograde degeneration study. J Comp Neurol 192: 377–385

    Google Scholar 

  • Steiger H-J, Büttner-Ennever JA (1979) Oculomotor nucleus afferents in the monkey demonstrated with horseradish peroxidase. Brain Res 160: 1–15

    Google Scholar 

  • Taber Pierce E (1975) Histogenesis of the deep cerebellar nuclei in the mouse: an autoradiographic study. Brain Res 95: 503–518

    Google Scholar 

  • Tolbert DL, Bantli H (1979) An HRP and autoradiographic study of cerebellar corticonuclear-nucleocortical reciprocity in the monkey. Exp Brain Res 36: 563–571

    Google Scholar 

  • Tolbert DL, Bantli H, Bloedel JR (1976) Anatomical and physiological evidence for a cerebellar nucleo-cortical projection in the cat. Neuroscience 1: 205–217

    Google Scholar 

  • Tolbert DL, Bantli H, Bloedel JR (1977) The intracerebellar nucleocortical projection in a primate. Exp Brain Res 30: 425–434

    Google Scholar 

  • Tolbert DL, Bantli H, Bloedel JR (1978a) Organizational features of the cat and monkey cerebellar nucleocortical projection. J Comp Neurol 182: 39–56

    Google Scholar 

  • Tolbert DL, Bantli H, Bloedel JR (1978b) Multiple branching of cerebellar efferent projections in cats. Exp Brain Res 31: 305–316

    Google Scholar 

  • Tolbert DL, Massopust LC, Murphy MG, Young PA (1976) The anatomical organization of the cerebello-olivary projection in the cat. J Comp Neurol 170: 525–544

    Google Scholar 

  • Verbitskaya LB (1969) Some aspects of the ontophylogenesis of the cerebellum. In: Llinás R (ed) Neurobiology of cerebellar evolution and development. Am Med Assoc Educ Res Found, Chicago, pp 859–874

    Google Scholar 

  • Voogd J (1969) The importance of fiber connections in the comparative anatomy of the mammalian cerebellum. In: Llinás R (ed) Neurobiology of cerebellar evolution and development. Am Med Assoc Educ Res Found, Chicago, pp 493–514

    Google Scholar 

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This work was supported by U.S.P.H.S. Grant NS 14841 and Postdoctoral Fellowship NS 06061

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Gould, B.B., Rakic, P. The total number, time of origin and kinetics of proliferation of neurons comprising the deep cerebellar nuclei in the rhesus monkey. Exp Brain Res 44, 195–206 (1981). https://doi.org/10.1007/BF00237341

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  • DOI: https://doi.org/10.1007/BF00237341

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