Advertisement

Anatomy and Embryology

, Volume 152, Issue 3, pp 273–289 | Cite as

Development of the interpeduncular nucleus in the midbrain of rhesus monkey and human

  • Nicholas J. Lenn
  • Neal Halfon
  • Pasko Rakic
Article

Summary

The development of the interpeduncular nucleus (IPN) in primates was studied in rhesus monkey with 3H-thymidine autoradiographic, Nissl and Golgi methods and in humans in histological preparations from embryos and fetuses of different ages. Autoradiographic analysis demonstrated that the neurons of the monkey IPN underwent their final cell division between postconception day 36 (E36) and E42, which corresponds to Stages 17 through 21 of Hendrickx and Sawyer. Autoradiograms of monkeys sacrificed at various short intervals following exposure to a pulse of 3H-thymidine showed that IPN neurons were generated in the proximity of the ventricular surface near the confluence of the 3rd ventricle and cerebral aqueduct, migrated ventrally along the midline and then spread laterally after reaching the ventral midbrain, where IPN was first recognized at E45 (Stage 23). The distribution of successively generated neurons in autoradiograms revealed caudal to rostral and lateral to medial spatio-temporal gradients. Differentiation of IPN neuronal size and development of Nissl substance began in rhesus monkey only after postmitotic cells had reached their destination and seemed to be pronounced mainly through E104. However, growth of the dendrites and elaboration of their side branches as seen in Golgi impregnations progressed gradually from E81 to birth (E165) and perhaps even later.

Analysis of histological preparations of a series of human embryos and fetuses was used to derive similar information indirectly, since the autoradiographic method cannot be applied to man. It was found that IPN neurons in human probably underwent their final division between Carnegie Stage 17 and 21. Similarly, as in monkey, postmitotic cells in human IPN displayed an inverted fountain pattern of cellular migration. IPN could first be delineated at Stage 23. There was evidence for both caudal to rostral and lateral to medial spatiotemporal gradients in the human, as in the monkey. Thus, in monkey and human, all IPN neurons are generated within the first quarter of intrauterine life and there is remarkable similarity in the timing, tempo and pattern of IPN neuronal differentiation in both species, indicating the validity of using non-human primates as an experimental model for understanding the development of this structure in man.

Key words

Nervous system Development Midbrain Interpeduncular nucleus Primates 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Angevine, J.B., Jr: Time of neuron origin in the hippocampal region. An autoradiographic study in the mouse. Exp. Neurol. Suppl. 2, 1–70 (1965)Google Scholar
  2. Bartelmez, G.W., Dekaban, A.S.: The early development of the human brain. Contr. Embryol. Carneg. Instn. 37, 13–32 (1962)Google Scholar
  3. Bruckner, G., Mares, V., Biesold, D.: Neurogenesis in the visual system of the rat. An autoradiographic investigation. J. Comp. Neur. 166, 245–256 (1976)Google Scholar
  4. Halfon, N., Lenn, N.J.: Prenatal development of the human interpeduncular nucleus. Neurosci. Absts. 2, 214 (1976)Google Scholar
  5. Hanaway, J., McConnell, J.A., Netsky, M.G.: Histogenesis of the substantia nigra, ventral tegmental area of Tsai and interpeduncular nucleus: an autoradiographic study of the mesencephalon in the rat. J. Comp. Neur. 142, 59–74 (1971)Google Scholar
  6. Hendrickx, A.G., Sawyer, R.H.: Embryology of the rhesus monkey. In: Rhesus monkey, Vol. II. Management, reproduction and pathology (G.B. Bourne, ed.) pp. 141–169. New York: Academic Press, 1975Google Scholar
  7. Herkenham, M., Nauta, W.J.H.: Projection of the habenular nuclei in the rat. Anat. Rec. 187, 603 (1977)Google Scholar
  8. Herrick, C.J.: The brain of the tiger salamander. p. 191–211. Chicago: University of Chicago Press, 1948Google Scholar
  9. Lenn, N.J.: Synapses in the interpeduncular nucleus: electron microscopy of normal and habenula lesioned rats. J. Comp. Neur. 166, 73–100 (1976)Google Scholar
  10. Lenn, N.J.: Postnatal synaptogenesis in the rat interpeduncular nucleus. J. Comp. Neur., (1977a) in pressGoogle Scholar
  11. Lenn, N.J.: Effect of neonatal deafferentation on synaptogenesis in the rat interpeduncular nucleus. J. Comp. Neur., (1977b) in pressGoogle Scholar
  12. Levitt, P., Moore, R.Y., Garber, B.B.: Selective cell association of catecholamine neurons in brain aggregates in vitro. Brain Res. 111, 311–320 (1976)Google Scholar
  13. O'Rahilly, R.: Developmental stages in human embryos. Part A: Embryos of the first three weeks (Stages 1 to 9). Contr. Carneg. Embryol. Instn., Publ. 631, 1–167 (1973)Google Scholar
  14. Pasquier, D.A., Anderson, C., Forbes, W.B., Morgane, P.J.: Horseradish peroxidase tracing of the lateral habenular-midbrain raphe nuclei connections in the rat. Brain Res. Bull. 1, 443–451 (1976)Google Scholar
  15. Rakic, P.: Neuron-glial relationship during granule cell migration in developing cerebellar cortex. A Golgi and electronmicroscopic study in Macacus rhesus. J. Comp. Neur. 141, 283–312 (1971)Google Scholar
  16. Rakic, P.: Kinetics of proliferation and latency between final cell division and onset of differentiation of cerebellar stellate and basket neurons. J. Comp. Neur. 147, 523–546 (1973)Google Scholar
  17. Rakic, P.: Timing of major ontogenetic events in the visual cortex of the rhesus monkey. In: Brain mechanisms in mental retardation (N.A. Buchwald and M. Brazier, eds.) pp. 3–40. New York: Academic Press (1975)Google Scholar
  18. Rakic, P.: 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. Neur. 176, 23–52 (1977)Google Scholar
  19. Ramon y Cajal, S.: Histologie du Systéme nerveux de l'homme et des vértébrés (Trans. by L. Azoulay) vol. 2, pp. 270–275. Paris: Maloine, 1909–1911Google Scholar
  20. Sidman, R.L.: Autoradiographic methods and principles for study of the nervous system with thymidine-H3. In: Contemporary research methods in neuroanatomy (W.J.H. Nauta and S.Q.E. Ebbeson, eds.), pp. 251–274. New York: Springer-Verlag, 1970Google Scholar
  21. Sidman, R.L., Rakic, P.: Neuronal migration, with special reference to developing human brain: a review. Brain Res. 62, 1–35 (1973)Google Scholar

Copyright information

© Springer-Verlag 1978

Authors and Affiliations

  • Nicholas J. Lenn
    • 1
    • 2
  • Neal Halfon
    • 1
    • 2
  • Pasko Rakic
    • 1
    • 2
  1. 1.Departments of Neurology and Pediatrics and Carnegie Laboratories of EmbryologyUniversity of CaliforniaDavis
  2. 2.Department of NeuropathologyHarvard Medical SchoolBoston

Personalised recommendations