Research report
Migration of dopaminergic neurons in the embryonic mesencephalon of mice

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Abstract

Migration of dopamine (DA)-containing neurons and its guiding cues were histologically examined in the embryonic mesencephalon of normal mice. Cells immunoreactive (ir) for tyrosine hydroxylase (TH), a DA-synthesizing enzyme, were first detected on embryonic day 10 (E10) in the medio-basal part of the mesencephalon and were distributed throughout the entire length of the ventral mesencephalic wall at E12. By E14, TH-ir cells were located laterally along the ventral pial surface to form the primordia of the substantia nigra. Experiments with a single injection of bromodeoxyuridine, a thymidine analog, demonstrated that cells generated in the ventricular surface of the ventral mesencephalon at E11 migrated ventrally and then moved laterally to form the substantia nigra and the ventral tegmental area. Electron microscopic examination of the ventral mesencephalon of E12 mice disclosed that in the dorsal part ventrally migrating immature neurons made close contacts with the processes of radial glial cells. The expression of tenascin was transiently seen on radial glial processes between E10 and E13 coincident with the period of the ventral migration of mesencephalic DA neurons. By double immunostaining of E13 mesencephalon, ventrally migrating TH-ir cells were seen to be apposed to tenascin-bearing radial glial processes. On the other hand, laterally migrating neurons in the basal part of the mesencephalon were observed by electron microscopy to contact with tangentially arranged nerve fibers which were immunopositive for the 160 kDa neurofilament polypeptide at the light microscopic level from E10. Double immunostaining of E13 mesencephalon demonstrated that laterally migrating TH-ir cells were intermingled among neurofilament-ir fiber bundles. The cells of origin of the tangential nerve fibers were detected in the lateral part of the mesencephalon, when a fluorescent dye, 1,1′-dioctadecyl-3,3,3′,3′-tetramethyl-indocarbocyanine perchlorate (DiI) was injected into the basal part of the mesencephalon of fixed E12 mice. The present results suggest that guiding cues of the radial migration of mesencephalic DA neurons represent processes of radial glial cells which express tenascin. On the other hand, tangentially arranged nerve fibers originating from the lateral part of the mesencephalon may provide a scaffolding along which the mesencephalic DA neurons subsequently migrate laterally to form the ventral tegmental area and the substantia nigra.

References (45)

  • R.L. Sidman et al.

    Neuronal migration, with special reference to developing human brain: a review

    Brain Res.

    (1973)
  • C.W. Shults et al.

    Dopaminergic cells align along radial glia in the developing mesencephalon of the rat

    Neuroscience

    (1990)
  • J. Spring et al.

    Two contrary functions of tenascin: Dissection of the active sites by recombinant tenascin fragments

    Cell

    (1989)
  • P. Voorn et al.

    The pre- and postnatal development of the dopaminergic cell groups in the ventral mesencephalon and the dopaminergic innervation of the striatum of the rat

    Neuroscience

    (1988)
  • J. Altman

    The early stage of nervous system development: neurogenesis and neuronal migration

  • A. Brodal

    Neurological Anatomy in Relation to Clinical Medicine

  • M. Bronner-Fraser

    Distribution and function of tenascin during cranial neural crest development in the chick

    J. Neurosci. Res.

    (1988)
  • C.-M. Chuong

    Differential roles of multiple adhesion molecules in cell migration: granule cell migration in cerebellum

    Experientia

    (1990)
  • C.-Y. Chuong et al.

    Sequential expression and differential function of multiple adhesion molecules during the formation of cerebellar cortical layers

    J. Cell Biol.

    (1987)
  • A. Dahlström et al.

    Evidence for the existence of monoamine-containing neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brain stem neurons

    Acta. Physiol. Scand.

    (1964)
  • U. Di porzio et al.

    Early appearance of tyrosine hydroxylase immunoreactive cells in the mesencephalon of mouse embryos

    Int. J. Dev. Neurosci.

    (1990)
  • P. Godement et al.

    A study in developing visual systems with a new method of staining neurones and their processes in fixed tissue

    Development

    (1987)
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