Home LiteratureArticle Details
PMID: 8627360 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The ganglionic eminence may be an intermediate target for corticofugal and thalamocortical axons.

Métin C, Godement P

Abstract

In the nervous system of many species, growing axons associate transiently with cellular groupings along their path. Whether this mechanism applies to the development of corticothalamic and thalamocortical projections is unknown. Using carbocyanine dyes, we studied the early growth of both corticofugal and thalamocortical fibers in hamster embryos. At embryonic day 11.5 (E11.5), corticofugal fibers invade the lateral ganglionic eminence (LGE), and thalamocortical fibers invade the medial ganglionic eminence (MGE). At this age, both sets of fibers are not yet in contact with each other. At the same time, neurons in each subdivision of the GE grow toward the cortex and thalamus. During the next 24 hr, corticofugal and thalamocortical fibers remain within the confines of the GE, where they course at different radial levels and bear large and complex growth cones. In the LGE, corticofugal fibers are often found in close association with cells that are likely to be neuronal. Starting on E13.5, both early projections from the GE decrease, and corticothalamic and thalamocortical fibers invade their definitive target regions. To test whether the GE specifically orients the growth and trajectories of cortical fibers even in the absence of the reciprocal thalamic projection, we cocultured explants of cortex and GE from either hamster or mouse embryos. These experiments showed that the GE, but not other tested brain regions, is able specifically to orient the growth of cortical axons. We therefore suggest that the GE may be an intermediate target in the pathfinding of axons between the cortex and the thalamus.

MeSH Terms
Animals Axons/physiology Cerebral Cortex/anatomy & histology Cricetinae Ganglia/anatomy & histology Immunohistochemistry Mice Mice, Inbred C57BL Neural Pathways/physiology Thalamus/anatomy & histology
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Métin C
Institut Alfred Fessard, Centre National de la Recherche Scientifique UPR 2212, Gif-sur-Yvette, France.
Godement P
References (61)
61 references, click to expand
  1. Pathfinding at the mammalian optic chiasm.
    Curr Opin Neurobiol. 1993 Feb;3(1):45-52 PMID: 8453289
  2. Dual origin of the mammalian neocortex and evolution of the cortical plate.
    Anat Embryol (Berl). 1978 Feb 20;152(2):109-26 PMID: 637312
  3. Differential reaction of crossing and non-crossing rat retinal axons on cell membrane preparations from the chiasm midline: an in vitro study.
    Development. 1993 Feb;117(2):725-35 PMID: 8330536
  4. Growth and targeting of subplate axons and establishment of major cortical pathways.
    J Neurosci. 1992 Apr;12(4):1194-211 PMID: 1556593
  5. TAG-1 can mediate homophilic binding, but neurite outgrowth on TAG-1 requires an L1-like molecule and beta 1 integrins.
    Neuron. 1994 Mar;12(3):675-90 PMID: 7512353
  6. A vertebrate gene related to orthodenticle contains a homeodomain of the bicoid class and demarcates anterior neuroectoderm in the gastrulating mouse embryo.
    EMBO J. 1993 Jul;12(7):2735-47 PMID: 8101484
  7. Requirement for subplate neurons in the formation of thalamocortical connections.
    Nature. 1990 Sep 13;347(6289):179-81 PMID: 2395469
  8. Postnatal development of striatal connections in the rat: a transport study with wheat germ agglutinin-horseradish peroxidase.
    Brain Res Dev Brain Res. 1990 Dec 1;57(1):43-53 PMID: 1708707
  9. Development of projection neuron types, axon pathways, and patterned connections of the mammalian cortex.
    Neuron. 1993 Jun;10(6):991-1006 PMID: 8318235
  10. Transient calbindin-D28k-positive systems in the telencephalon: ganglionic eminence, developing striatum and cerebral cortex.
    J Neurosci. 1992 Feb;12(2):674-90 PMID: 1740695
  11. The early development of thalamocortical and corticothalamic projections.
    J Comp Neurol. 1993 Sep 1;335(1):16-41 PMID: 8408772
  12. Cells and cell-interactions that guide motor axons in the developing chick embryo.
    Bioessays. 1991 Jan;13(1):17-23 PMID: 1772406
  13. DLX-2, MASH-1, and MAP-2 expression and bromodeoxyuridine incorporation define molecularly distinct cell populations in the embryonic mouse forebrain.
    J Neurosci. 1994 Nov;14(11 Pt 1):6370-83 PMID: 7965042
  14. Axon guidance and the patterning of neuronal projections in vertebrates.
    Science. 1988 Nov 4;242(4879):692-9 PMID: 3055291
  15. Development of GABA-immunoreactivity in the neocortex of the mouse.
    J Comp Neurol. 1992 Dec 22;326(4):501-26 PMID: 1484122
  16. Neurogenesis in the basal forebrain in the Chinese hamster (cricetulus griseus). II. Site of neuron origin: morphogenesis of the ventricular ridges.
    Anat Embryol (Berl). 1980;158(2):193-211 PMID: 7356177
  17. Growth cone morphology and trajectory in the lumbosacral region of the chick embryo.
    J Neurosci. 1985 Sep;5(9):2345-58 PMID: 4032000
  18. A study in developing visual systems with a new method of staining neurones and their processes in fixed tissue.
    Development. 1987 Dec;101(4):697-713 PMID: 2460302
  19. Calbindin (CaBP 28 kDa) appearance and distribution during development of the mouse inner ear.
    Brain Res. 1988 May 16;468(2):233-42 PMID: 3260120
  20. Specification of cerebral cortical areas.
    Science. 1988 Jul 8;241(4862):170-6 PMID: 3291116
  21. Pathfinding and target selection by developing geniculocortical axons.
    J Neurosci. 1992 Jan;12(1):39-55 PMID: 1729444
  22. Developmental mechanisms that generate precise patterns of neuronal connectivity.
    Cell. 1993 Jan;72 Suppl:77-98 PMID: 8428376
  23. Retinal axon pathfinding in the optic chiasm: divergence of crossed and uncrossed fibers.
    Neuron. 1990 Aug;5(2):173-86 PMID: 2383400
  24. Neurogenesis in the visual system of the rat. An autoradiographic investigation.
    J Comp Neurol. 1976 Mar 15;166(2):245-55 PMID: 1262556
  25. Mode of cell migration to the superficial layers of fetal monkey neocortex.
    J Comp Neurol. 1972 May;145(1):61-83 PMID: 4624784
  26. Early events in the embryogenesis of the vertebrate visual system: cellular determination and pathfinding.
    Annu Rev Neurosci. 1990;13:155-69 PMID: 2183672
  27. Visual cortex development in the ferret. I. Genesis and migration of visual cortical neurons.
    J Neurosci. 1989 Apr;9(4):1242-53 PMID: 2703875
  28. The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6.
    Cell. 1994 Aug 12;78(3):409-24 PMID: 8062384
  29. Development of the thalamic reticular and perireticular nuclei in rats and their relationship to the course of growing corticofugal and corticopetal axons.
    J Comp Neurol. 1993 Dec 22;338(4):575-87 PMID: 8132862
  30. Pioneer growth cone steering along a series of neuronal and non-neuronal cues of different affinities.
    J Neurosci. 1986 Jun;6(6):1781-95 PMID: 3712010
  31. Neurogenesis of the cat's primary visual cortex.
    J Comp Neurol. 1985 Dec 22;242(4):611-31 PMID: 4086673
  32. Chemotropic guidance of developing axons in the mammalian central nervous system.
    Nature. 1988 Dec 22-29;336(6201):775-8 PMID: 3205306
  33. Peripheral pathways are pioneered by an array of central and peripheral neurones in grasshopper embryos.
    Nature. 1982 Jun 3;297(5865):404-6 PMID: 6176880
  34. Optical microscopy. 3. Tracking fluorescently labeled neurons in developing brain.
    FASEB J. 1995 Mar;9(5):324-34 PMID: 7896001
  35. Retinal axon divergence in the optic chiasm: uncrossed axons diverge from crossed axons within a midline glial specialization.
    J Neurosci. 1995 May;15(5 Pt 2):3716-29 PMID: 7751940
  36. Guidance of developing axons by diffusible chemoattractants.
    Cold Spring Harb Symp Quant Biol. 1990;55:279-89 PMID: 2132821
  37. Retinal axon divergence in the optic chiasm: dynamics of growth cone behavior at the midline.
    J Neurosci. 1994 Nov;14(11 Pt 2):7024-39 PMID: 7965096
  38. Neurogenesis in the central visual pathways of the golden hamster.
    Brain Res. 1982 Sep;281(1):99-103 PMID: 7139343
  39. Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse.
    Nature. 1961 Nov 25;192:766-8 PMID: 17533671
  40. A pioneering growth cone in the embryonic zebrafish brain.
    Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2293-6 PMID: 2006169
  41. Pathfinding by neuronal growth cones in grasshopper embryos. II. Selective fasciculation onto specific axonal pathways.
    J Neurosci. 1983 Jan;3(1):31-41 PMID: 6822859
  42. Cell proliferation, migration and differentiation in the cerebral cortex of the golden hamster.
    J Comp Neurol. 1970 Jun;139(2):227-44 PMID: 5422533
  43. The migration of neuroblasts in the developing cerebral cortex.
    J Anat. 1965 Oct;99(Pt 4):691-709 PMID: 5325778
  44. The neostriatal mosaic: multiple levels of compartmental organization.
    Trends Neurosci. 1992 Apr;15(4):133-9 PMID: 1374971
  45. Guidance of cerebellofugal axons in the rat embryo: directed growth toward the floor plate and subsequent elongation along the longitudinal axis.
    Neuron. 1995 May;14(5):961-72 PMID: 7748563
  46. Dynamic structure of the radial glial fiber system of the developing murine cerebral wall. An immunocytochemical analysis.
    Brain Res Dev Brain Res. 1989 Nov 1;50(1):55-67 PMID: 2582608
  47. New views of the thalamic reticular nucleus in the adult and the developing brain.
    Trends Neurosci. 1993 Jun;16(6):240-5 PMID: 7688166
  48. Development of the thalamic reticular nucleus in ferrets with special reference to the perigeniculate and perireticular cell groups.
    Eur J Neurosci. 1994 Feb 1;6(2):253-63 PMID: 7513240
  49. Mechanisms of axonal guidance used by interneurons in the chick embryo spinal cord.
    Perspect Dev Neurobiol. 1993;1(4):205-15 PMID: 8087545
  50. Development of layer I and the subplate in the rat neocortex.
    Exp Neurol. 1990 Jan;107(1):48-62 PMID: 2295319
  51. Spatially restricted expression of Dlx-1, Dlx-2 (Tes-1), Gbx-2, and Wnt-3 in the embryonic day 12.5 mouse forebrain defines potential transverse and longitudinal segmental boundaries.
    J Neurosci. 1993 Jul;13(7):3155-72 PMID: 7687285
  52. Both adult and juvenile tau microtubule-associated proteins are axon specific in the developing and adult rat cerebellum.
    Neuroscience. 1988 Apr;25(1):139-46 PMID: 3134623
  53. Factors involved in the establishment of specific interconnections between thalamus and cerebral cortex.
    Cold Spring Harb Symp Quant Biol. 1990;55:491-504 PMID: 2132833
  54. Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon.
    J Neurosci. 1994 Sep;14(9):5399-416 PMID: 8083744
  55. How do thalamic axons find their way to the cortex?
    Trends Neurosci. 1995 Sep;18(9):389-97 PMID: 7482804
  56. Growth cone morphology varies with position in the developing mouse visual pathway from retina to first targets.
    J Neurosci. 1987 May;7(5):1447-60 PMID: 3572487
  57. Prenatal development of the intrinsic neurons of the rat neocortex: a comparative study of the distribution of GABA-immunoreactive cells and the GABAA receptor.
    Neuroscience. 1991;40(2):375-97 PMID: 1851254
  58. Subplate neurons pioneer the first axon pathway from the cerebral cortex.
    Science. 1989 Sep 1;245(4921):978-82 PMID: 2475909
  59. The subplate, a transient neocortical structure: its role in the development of connections between thalamus and cortex.
    Annu Rev Neurosci. 1994;17:185-218 PMID: 8210173
  60. Precocious pathfinding: retinal axons can navigate in an axonless brain.
    Neuron. 1992 Dec;9(6):1001-11 PMID: 1281416
  61. Embryonic neurons of the developing optic chiasm express L1 and CD44, cell surface molecules with opposing effects on retinal axon growth.
    Neuron. 1994 May;12(5):957-75 PMID: 7514428
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1996-05-15
Pages
3219-35
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6579142
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]