Summary
Migration of neuronal cells in the subpial part of the medulla oblongata was examined in the fetal mouse by light and electron microscopy. Cells were observed forming a migratory stream in the period between the thirteenth and sixteenth days of gestation, and were associated with tangentially oriented fibers. Many of these tangential fibers were present prior to the onset of the migration, and the fibers were filled with longitudinally arrayed microtubules. The cell-bodies were elongated and arranged along, and often apposed to the fibers. Some relocating neurons extended fibers, i.e. leading processes, in the direction of the migration. Generally, these cells exhibited features of immature neurons; they displayed a high concentration of ribosomal rosettes and contained mitochondria, Golgi apparatus, a few rough endoplasmic reticula, and occasionally, centrioles. Junctional complexes, coated pits and coated vesicles were frequently observed in the region of the migratory stream, and these structures are considered to be related to cell locomotion. The present findings strongly suggest that such tangential fibers, including leading processes of moving neurons, serve as guidance substrates for the relocation of immature neurons in the mouse subpial medullary region.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Altman J, Bayer SA (1978) Prenatal development of the cerebellar system in the rat. II. Cytogenesis and histogenesis of the inferior olive, pontine gray and the precerebellar reticular nuclei. J Comp Neurol 179:49–76
Altman J, Bayer SA (1987a) Development of the precerebellar nuclei in the rat. I. The precerebellar neuroepithelium of the rhombencephalon. J Comp Neurol 257:477–489
Altman J, Bayer SA (1987b) Development of the precerebellar nuclei in the rat. II. The intramural olivary migratory stream and the neurogenetic organization of the inferior olive. J Comp Neurol 257:490–512
Altman J, Bayer SA (1987c) Development of the precerebellar nuclei in the rat. III. The posterior precerebellar extramural migratory stream and the lateral reticular and external cuneate nuclei. J Comp Neurol 257:513–528
Altman J, Bayer SA (1987d) Development of the precerebellar nuclei in the rat. IV. The anterior precerebellar extramural migratory stream and the nucleus reticularis tegmenti pontis and the basal pontine gray. J Comp Neurol 257:529–552
Boulder Committee (1970) Embryonic vertebrate central nervous system: revised terminology. Anat Rec 166:257–262
Bourrat F, Sotelo C (1988) Migratory pathways and neuritic differentiation of inferior olivary neurons in the rat embryo: axonal tracing study using the in vitro slab technique. Dev Brain Res 39:19–37
Bretscher MS (1984) Endocytosis: relation to capping and cell locomotion. Science 224:681–686
Chuong C-M, Crossin KL, Edelman GM (1987) Sequential expression and differential function of multiple adhesion molecules during the formation of cerebellar cortical layers. J Cell Biol 104:331–342
Das GD, Lammert GL, McAllister JP (1974) Contact guidance and migratory cells in the developing cerebellum. Brain Res 69:13–29
Ellenberger C Jr, Hanaway J, Netsky MG (1969) Embryogenesis of the inferior olivary nucleus in the rat: a radioautographic study and a re-evaluation of the rhombic lip. J Comp Neurol 137:71–88
Essick CR (1912) The development of the nuclei pontis and the nucleus arcuatus in man. Am J Anat 13:25–54
Fujita S (1963) The matrix cell and cytogenesis in the developing central nervous system. J Comp Neurol 120:37–42
Handley DA, Arbeeny CM, Witte LD, Chien S (1981) Colloidal gold-low density lipoprotein conjugates as membrane receptor probes. Proc Natl Acad Sci USA 78:368–371
Harkmark W (1954) Cell migrations from the rhombic lip to the inferior olive, the nucleus raphe and the pons: a morphological and experimental investigation on chick embryos. J Comp Neurol 100:115–209
His W (1890) Die Entwickelung des menschlichen Rautenhirns vom Ende des ersten bis zum Beginn des dritten Monats. I. Verlängertes Mark. Abh Kgl Sachs Ges, Wissensch Math Phys Kl 17:1–74
Hynes RO, Patel R, Miller RH (1986) Migration of neuroblasts along preexisting axonal tracts during prenatal cerebellar development. J Neurosci 6:867–876
Krystosek A, Seeds NW (1981) Plasminogen activator release at the neuronal growth cone. Science 213:1532–1534
Letourneau PC, Wessells NK (1974) Migratory cell locomotion versus nerve axon elongation: differences based on the effects of lanthanum ion. J Cell Biol 61:56–69
Lindner J, Rathjen FG, Schachner M (1983) L1 mono- and polyclonal antibodies modify cell migration in early postnatal mouse cerebellum. Nature 305:427–430
Meller K, Glees P (1969) The development of the mouse cerebellum: a Golgi and electron microscopical study. In: Llinas R (ed) Neurobiology of cerebellar evolution and development. Am Med Assn Educ Res Fed, Chicago, pp 783–801
Meller K, Breipohl W, Glees P (1966) Early cytological differentiation in the cerebral hemisphere of mice: an electronmicroscopical study. Z Zellforsch 72:525–533
Moody SA, Heaton MB (1983) Ultrastructural observation of the migration and early development of trigeminal motoneurons in chick embryos. J Comp Neurol 216:20–35
Moonen G, Grau-Wagemans MP, Selak I (1982) Plasminogen activator-plasmin system and neuronal migration. Nature 298:753–755
Murakami T (1973) A metal impregnation method of biological specimens for scanning electron microscopy. Arch Histol Jpn 35:323–326
Nowakowski RS, Rakic P (1979) The mode of migration of neurons to the hippocampus: a Golgi and electron microsopic analysis in foetal rhesus monkey. J Neurocytol 8:697–718
Palmgren A (1948) A rapid method for selective silver staining of nerve fibers and nerve endings in mounted paraffin sections. Act Zool 29:377–392
Peters A, Feldman M (1973) The cortical plate and molecular layer of the late rat fetus. Z Anat Entwickl -Gesch 141:3–37
Privat A (1974) A possible mechanism for the resorption of attachment plates in the growing rat brain. Brain Res 69:125–129
Puelles L, Privat A (1977) Do oculomotor neuroblasts migrate across the midline in the fetal rat brain? Anat Embryol 150:187–206
Rakic P (1971a) Guidance of neurons migrating to the fetal monkey neocortex. Brain Res 33:471–476
Rakic P (1971b) Neuron-glia relationship during granule cell migration in developing cerebellar cortex: a Golgi and electronmicroscopic study in Macacus rhesus. J Comp Neurol 141:283–312
Rakic P (1972) Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 145:61–84
Rakic P (1985) Contact regulation of neuronal migration. In: Edelman GM, Thiery J-P (eds) The cell in contact. John Wiley and Sons, New York, pp 67–91
Sidman RL, Rakic P (1973) Neuronal migration, with special reference to developing human brain: a review. Brain Res 62:1–35
Strassman RJ, Letourneau PC, Wessells NK (1973) Elongation of axons in an agar matrix that dose not support cell locomotion. Exp Cell Res 81:482–487
Swarz JR, Oster-Granite ML (1978) Presence of radial glia in foetal mouse cerebellum. J Neurocytol 7:301–312
Taber-Pierce E (1966) Histogenesis of the nuclei griseum pontis, corporis pontobulbaris and reticularis tegmenti pontis (Bechterew) in the mouse: an autoradiographic study. J Comp Neurol 126:219–240
Trinkaus JP, (1985) Further thoughts on directional cell movement during morphogenesis. J Neurosci Res 13:1–19
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Ono, K., Kawamura, K. Migration of immature neurons along tangentially oriented fibers in the subpial part of the fetal mouse medulla oblongata. Exp Brain Res 78, 290–300 (1989). https://doi.org/10.1007/BF00228900
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00228900