Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Modes of neuronal migration in the developing cerebral cortex

Nature Reviews Neuroscience volume 3, pages 423–432 (2002)Cite this article

Key Points

  • In the developing nervous system, two modes of migration have been identified: radial and tangential. Radial migration is the principal mode of migration in the developing cerebral cortex, although the GABA (γ-aminobutyric acid)-expressing interneurons, which arise in the ventral telencephalon, migrate tangentially into the cortex.

  • Layers II–VI of the mammalian cortex are generated in an 'inside-out' sequence, such that early-born cells reside in the deepest layers, whereas later-born cells migrate past the existing layers to form the superficial layers.

  • Radially migrating neurons adopt two separate modes of movement: somal translocation during the early stages of corticogenesis; and glia-guided migration during the later stages, when the cerebral wall is considerably thicker.

  • Evidence for somal translocation came from the reeler mouse and from other mutants that have abnormal cortical lamination. Although these mutations disrupt glia-guided migration, the preplate forms normally, indicating that another mode of radial migration is required for the early stages of cortical lamination.

  • Translocation might be an older mode of movement in the evolution of the cerebral cortex for the transfer of preplate and early cortical-plate neurons, whereas glia-guided migration might have evolved to guide cells across more complex paths during late corticogenesis.

  • Little is known about how tangentially migrating interneurons integrate into specific cortical layers. A recent study has shown that they migrate towards the cortical ventricular zone, a mode of movement termed 'ventricle-directed migration'. Here, they might receive layer information that is essential for their correct integration. The next challenge will be to establish where they acquire spatial information, and what signals guide them to their correct positions.

Abstract

The conventional scheme of cortical formation shows that postmitotic neurons migrate away from the germinal ventricular zone to their positions in the developing cortex, guided by the processes of radial glial cells. However, recent studies indicate that different neuronal types adopt distinct modes of migration in the developing cortex. Here, we review evidence for two modes of radial movement: somal translocation, which is adopted by the early-generated neurons; and glia-guided locomotion, which is used predominantly by pyramidal cells. Cortical interneurons, which originate in the ventral telencephalon, use a third mode of migration. They migrate tangentially into the cortex, then seek the ventricular zone before moving radially to take up their positions in the cortical anlage.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Neocortical development.
Figure 2: Models of cortical neuronal migration.
Figure 3: Somal translocation.
Figure 4: Glia-guided migration.
Figure 5: Ventricle-directed migration.
Figure 6: Movement of cortical interneurons in the developing cerebral cortex.

Similar content being viewed by others

References

  1. Gleeson, J. G. & Walsh, C. A. Neuronal migration disorders: from genetic diseases to developmental mechanisms. Trends Neurosci. 23, 352–359 (2000).

    CAS  PubMed  Google Scholar 

  2. Lambert de Rouvroit, C. & Goffinet, A. M. Neuronal migration. Mech. Dev. 105, 47–56 (2001).

    CAS  PubMed  Google Scholar 

  3. Ross, M. E. & Walsh, C. A. Human brain malformations and their lessons for neuronal migration. Annu. Rev. Neurosci. 24, 1041–1070 (2001).A review of studies that point to neuronal migration disorders in human brain malformations.

    CAS  PubMed  Google Scholar 

  4. Hatten, M. E. Central nervous system neuronal migration. Annu. Rev. Neurosci. 22, 511–539 (1999).

    CAS  PubMed  Google Scholar 

  5. Parnavelas, J. G. The origin and migration of cortical neurones: new vistas. Trends Neurosci. 23, 126–131 (2000).

    CAS  PubMed  Google Scholar 

  6. Marin, O. & Rubenstein, J. L. A long, remarkable journey: tangential migration in the telencephalon. Nature Rev. Neurosci. 2, 780–790 (2001).A comprehensive review of the genetic mechanisms involved in the tangential migration of cortical interneurons from the ventral telencephalon.

    CAS  Google Scholar 

  7. Wilson, S. W. & Rubenstein, J. L. Induction and dorsoventral patterning of the telencephalon. Neuron 28, 641–651 (2000).

    CAS  PubMed  Google Scholar 

  8. Uylings, H. B., Van Eden, C. G., Parnavelas, J. G. & Kalsbeek, A. in The Cerebral Cortex of the Rat (eds Kolb, B. & Tees, R. C.) 35–76 (MIT Press, Cambridge, Massachusetts, 1990).

    Google Scholar 

  9. Angevine, J. B. & Sidman, R. L. Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192, 766–768 (1961).

    PubMed  Google Scholar 

  10. Berry, M. & Rogers, A. W. The migration of neuroblasts in the developing cerebral cortex. J. Anat. 99, 691–709 (1965).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Rakic, P. Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neurol. 145, 61–83 (1972).

    CAS  PubMed  Google Scholar 

  12. Rakic, P., Stensas, L. J., Sayre, E. & Sidman, R. L. Computer-aided three-dimensional reconstruction and quantitative analysis of cells from serial electron microscopic montages of foetal monkey brain. Nature 250, 31–34 (1974).

    CAS  PubMed  Google Scholar 

  13. Walsh, C. & Cepko, C. L. Clonal dispersion in proliferative layers of developing cerebral cortex. Nature 362, 632–635 (1993).

    CAS  PubMed  Google Scholar 

  14. Mione, M. C., Cavanagh, J. F., Harris, B. & Parnavelas, J. G. Cell fate specification and symmetrical/asymmetrical divisions in the developing cerebral cortex. J. Neurosci. 17, 2018–2029 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Tan, S. S. et al. Cell dispersion patterns in different cortical regions studied with an X-inactivated transgenic marker. Development 121, 1029–1039 (1995).

    CAS  PubMed  Google Scholar 

  16. Tan, S. S. et al. Separate progenitors for radial and tangential cell dispersion during development of the cerebral neocortex. Neuron 21, 295–304 (1998).

    CAS  PubMed  Google Scholar 

  17. Nadarajah, B., Alifragis, P., Wong, R. O. & Parnavelas, J. G. Ventricle-directed migration in the developing cerebral cortex. Nature Neurosci. 5, 218–224 (2002).The first evidence of ventricle-directed migration in the developing cortex.

    CAS  PubMed  Google Scholar 

  18. Morest, D. K. A study of neurogenesis in the forebrain of opossum pouch young. Z. Anat. Entwicklungsgesch. 130, 265–305 (1970).The first anatomical evidence of somal translocation as a distinct mode of migration in the developing cortex.

    CAS  PubMed  Google Scholar 

  19. Brittis, P. A., Meiri, K., Dent, E. & Silver, J. The earliest patterns of neuronal differentiation and migration in the mammalian central nervous system. Exp. Neurol. 134, 1–12 (1995).

    CAS  PubMed  Google Scholar 

  20. Sidman, R. L. & Rakic, P. Neuronal migration, with special reference to developing human brain: a review. Brain Res. 62, 1–35 (1973).

    CAS  PubMed  Google Scholar 

  21. O'Rourke, N. A., Dailey, M. E., Smith, S. J. & McConnell, S. K. Diverse migratory pathways in the developing cerebral cortex. Science 258, 299–302 (1992).The first direct evidence of tangential movement of cortical neurons in vitro.

    CAS  PubMed  Google Scholar 

  22. Rakic, P. 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 (1971).

    CAS  PubMed  Google Scholar 

  23. Nowakowski, R. S. & Rakic, P. The site of origin and route and rate of migration of neurons to the hippocampal region of the rhesus monkey. J. Comp. Neurol. 196, 129–154 (1981).

    CAS  PubMed  Google Scholar 

  24. Shoukimas, G. M. & Hinds, J. W. The development of the cerebral cortex in the embryonic mouse: an electron microscopic serial section analysis. J. Comp. Neurol. 179, 795–830 (1978).

    CAS  PubMed  Google Scholar 

  25. Caviness, V. S. Jr & Rakic, P. Mechanisms of cortical development: a view from mutations in mice. Annu. Rev. Neurosci. 1, 297–326 (1978).

    PubMed  Google Scholar 

  26. Sweet, H. O., Bronson, R. T., Johnson, K. R., Cook, S. A. & Davisson, M. T. Scrambler, a new neurological mutation of the mouse with abnormalities of neuronal migration. Mamm. Genome 7, 798–802 (1996).

    CAS  PubMed  Google Scholar 

  27. Howell, B. W., Hawkes, R., Soriano, P. & Cooper, J. A. Neuronal position in the developing brain is regulated by mouse disabled-1. Nature 389, 733–737 (1997).

    CAS  PubMed  Google Scholar 

  28. Trommsdorff, M. et al. Reeler/disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97, 689–701 (1999).

    CAS  PubMed  Google Scholar 

  29. Gilmore, E. C., Ohshima, T., Goffinet, A. M., Kulkarni, A. B. & Herrup, K. Cyclin-dependent kinase 5-deficient mice demonstrate novel developmental arrest in cerebral cortex. J. Neurosci. 18, 6370–6377 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Chae, T. et al. Mice lacking p35, a neuronal specific activator of Cdk5, display cortical lamination defects, seizures, and adult lethality. Neuron 18, 29–42 (1997).

    CAS  PubMed  Google Scholar 

  31. Nadarajah, B., Brunstrom, J. E., Grutzendler, J., Wong, R. O. & Pearlman, A. L. Two modes of radial migration in early development of the cerebral cortex. Nature Neurosci. 4, 143–150 (2001).The first real-time evidence of somal translocation in the developing cortex.

    CAS  PubMed  Google Scholar 

  32. Miyata, T., Kawaguchi, A., Okano, H. & Ogawa, M. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31, 727–741 (2001).

    CAS  PubMed  Google Scholar 

  33. Noctor, S. C., Flint, A. C., Weissman, T. A., Dammerman, R. S. & Kriegstein, A. R. Neurons derived from radial glial cells establish radial units in neocortex. Nature 409, 714–720 (2001).

    CAS  PubMed  Google Scholar 

  34. Hartfuss, E., Galli, R., Heins, N. & Gotz, M. Characterization of CNS precursor subtypes and radial glia. Dev. Biol. 229, 15–30 (2001).Reference 32–34 provided the first direct evidence that radial glia give rise to cortical neurons.

    CAS  PubMed  Google Scholar 

  35. Parnavelas, J. G. & Nadarajah, B. Radial glial cells. Are they really glia? Neuron 31, 881–884 (2001).

    CAS  PubMed  Google Scholar 

  36. de Curtis, I. Cell migration: GAPs between membrane traffic and the cytoskeleton. EMBO Rep. 2, 277–281 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Ridley, A. J. Rho GTPases and cell migration. J. Cell Sci. 114, 2713–2722 (2001).

    CAS  PubMed  Google Scholar 

  38. Morris, N. R., Efimov, V. P. & Xiang, X. Nuclear migration, nucleokinesis and lissencephaly. Trends Cell Biol. 8, 467–470 (1998).

    CAS  PubMed  Google Scholar 

  39. Oakley, B. R. & Morris, N. R. Nuclear movement is β-tubulin-dependent in Aspergillus nidulans. Cell 19, 255–262 (1980).

    CAS  PubMed  Google Scholar 

  40. Oakley, B. R. & Morris, N. R. A β-tubulin mutation in Aspergillus nidulans that blocks microtubule function without blocking assembly. Cell 24, 837–845 (1981).

    CAS  PubMed  Google Scholar 

  41. Xiang, X., Zuo, W., Efimov, V. P. & Morris, N. R. Isolation of a new set of Aspergillus nidulans mutants defective in nuclear migration. Curr. Genet. 35, 626–630 (1999).

    CAS  PubMed  Google Scholar 

  42. Xiang, X., Osmani, A. H., Osmani, S. A., Xin, M. & Morris, N. R. NudF, a nuclear migration gene in Aspergillus nidulans, is similar to the human LIS-1 gene required for neuronal migration. Mol. Biol. Cell 6, 297–310 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Dobyns, W. B., Reiner, O., Carrozzo, R. & Ledbetter, D. H. Lissencephaly. A human brain malformation associated with deletion of the LIS1 gene located at chromosome 17p13. JAMA 270, 2838–2842 (1993).

    CAS  PubMed  Google Scholar 

  44. Hattori, M., Adachi, H., Tsujimoto, M., Arai, H. & Inoue, K. Miller–Dieker lissencephaly gene encodes a subunit of brain platelet-activating factor acetylhydrolase. Nature 370, 216–218 (1994).

    CAS  PubMed  Google Scholar 

  45. Leventer, R. J., Cardoso, C., Ledbetter, D. H. & Dobyns, W. B. LIS1: from cortical malformation to essential protein of cellular dynamics. Trends Neurosci. 24, 489–492 (2001).

    CAS  PubMed  Google Scholar 

  46. Wynshaw-Boris, A. & Gambello, M. J. LIS1 and dynein motor function in neuronal migration and development. Genes Dev. 15, 639–651 (2001).

    CAS  PubMed  Google Scholar 

  47. Hirotsune, S. et al. Graded reduction of Pafah1b1 (Lis1) activity results in neuronal migration defects and early embryonic lethality. Nature Genet. 19, 333–339 (1998).

    CAS  PubMed  Google Scholar 

  48. Cahana, A. et al. Targeted mutagenesis of Lis1 disrupts cortical development and LIS1 homodimerization. Proc. Natl Acad. Sci. USA 98, 6429–6434 (2001).References 47 and 48 provided the first evidence for an involvement of LIS1 in neuronal migration.

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Rivas, R. J. & Hatten, M. E. Motility and cytoskeletal organization of migrating cerebellar granule neurons. J. Neurosci. 15, 981–989 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Fox, J. W. et al. Mutations in filamin 1 prevent migration of cerebral cortical neurons in human periventricular heterotopia. Neuron 21, 1315–1325 (1998).

    CAS  PubMed  Google Scholar 

  51. Loo, D. T., Kanner, S. B. & Aruffo, A. Filamin binds to the cytoplasmic domain of the β1-integrin. Identification of amino acids responsible for this interaction. J. Biol. Chem. 273, 23304–23312 (1998).

    CAS  PubMed  Google Scholar 

  52. Sharma, C. P., Ezzell, R. M. & Arnaout, M. A. Direct interaction of filamin (ABP-280) with the β2-integrin subunit CD18. J. Immunol. 154, 3461–3470 (1995).

    CAS  PubMed  Google Scholar 

  53. Anton, E. S., Kreidberg, J. A. & Rakic, P. Distinct functions of α3 and αv integrin receptors in neuronal migration and laminar organization of the cerebral cortex. Neuron 22, 277–289 (1999).

    CAS  PubMed  Google Scholar 

  54. Fox, J. W. & Walsh, C. A. Periventricular heterotopia and the genetics of neuronal migration in the cerebral cortex. Am. J. Hum. Genet. 65, 19–24 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Nikolic, M., Chou, M. M., Lu, W., Mayer, B. J. & Tsai, L. H. The p35/Cdk5 kinase is a neuron-specific Rac effector that inhibits Pak1 activity. Nature 395, 194–198 (1998).

    CAS  PubMed  Google Scholar 

  56. Kwon, Y. T., Gupta, A., Zhou, Y., Nikolic, M. & Tsai, L. H. Regulation of N-cadherin-mediated adhesion by the p35–Cdk5 kinase. Curr. Biol. 10, 363–372 (2000).

    CAS  PubMed  Google Scholar 

  57. Redies, C. & Takeichi, M. Expression of N-cadherin mRNA during development of the mouse brain. Dev. Dyn. 197, 26–39 (1993).

    CAS  PubMed  Google Scholar 

  58. Rakic, P., Knyihar-Csillik, E. & Csillik, B. Polarity of microtubule assemblies during neuronal cell migration. Proc. Natl Acad. Sci. USA 93, 9218–9222 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Feng, Y. et al. LIS1 regulates CNS lamination by interacting with mNudE, a central component of the centrosome. Neuron 28, 665–679 (2000).

    CAS  PubMed  Google Scholar 

  60. Niethammer, M. et al. NUDEL is a novel Cdk5 substrate that associates with LIS1 and cytoplasmic dynein. Neuron 28, 697–711 (2000).

    CAS  PubMed  Google Scholar 

  61. Feng, Y. & Walsh, C. A. Protein–protein interactions, cytoskeletal regulation and neuronal migration. Nature Rev. Neurosci. 2, 408–416 (2001).

    CAS  Google Scholar 

  62. Rio, C., Rieff, H. I., Qi, P., Khurana, T. S. & Corfas, G. Neuregulin and erbB receptors play a critical role in neuronal migration. Neuron 19, 39–50 (1997).

    CAS  PubMed  Google Scholar 

  63. Anton, E. S., Marchionni, M. A., Lee, K. F. & Rakic, P. Role of GGF/neuregulin signaling in interactions between migrating neurons and radial glia in the developing cerebral cortex. Development 124, 3501–3510 (1997).

    CAS  PubMed  Google Scholar 

  64. Pearlman, A. L., Faust, P. L., Hatten, M. E. & Brunstrom, J. E. New directions for neuronal migration. Curr. Opin. Neurobiol. 8, 45–54 (1998).

    CAS  PubMed  Google Scholar 

  65. Rice, D. S. & Curran, T. Mutant mice with scrambled brains: understanding the signaling pathways that control cell positioning in the CNS. Genes Dev. 13, 2758–2773 (1999).

    CAS  PubMed  Google Scholar 

  66. Rice, D. S. & Curran, T. Role of the reelin signaling pathway in central nervous system development. Annu. Rev. Neurosci. 24, 1005–1039 (2001).References 65 and 66 are comprehensive reviews of the role of reelin and its signalling pathways in the developing nervous system.

    CAS  PubMed  Google Scholar 

  67. D'Arcangelo, G. & Curran, T. Reeler: new tales on an old mutant mouse. Bioessays 20, 235–244 (1998).

    CAS  PubMed  Google Scholar 

  68. Dulabon, L. et al. Reelin binds α3β1 integrin and inhibits neuronal migration. Neuron 27, 33–44 (2000).

    Article  CAS  PubMed  Google Scholar 

  69. Magdaleno, S., Keshvara, L. & Curran, T. Rescue of ataxia and preplate splitting by ectopic expression of reelin in reeler mice. Neuron 33, 573–586 (2002).

    CAS  PubMed  Google Scholar 

  70. Goffinet, A. M., Daumerie, C., Langerwerf, B. & Pieau, C. Neurogenesis in reptilian cortical structures: 3H-thymidine autoradiographic analysis. J. Comp. Neurol. 243, 106–116 (1986).

    CAS  PubMed  Google Scholar 

  71. Tsai, H. M., Garber, B. B. & Larramendi, L. M. 3H-Thymidine autoradiographic analysis of telencephalic histogenesis in the chick embryo. I. Neuronal birthdates of telencephalic compartments in situ. J. Comp. Neurol. 198, 275–292 (1981).

    CAS  PubMed  Google Scholar 

  72. Bar, I., Lambert de Rouvroit, C. & Goffinet, A. M. The evolution of cortical development. An hypothesis based on the role of the reelin signaling pathway. Trends Neurosci. 23, 633–638 (2000).

    CAS  PubMed  Google Scholar 

  73. Marin-Padilla, M. Dual origin of the mammalian neocortex and evolution of the cortical plate. Anat. Embryol. (Berl.) 152, 109–126 (1978).

    CAS  Google Scholar 

  74. Goffinet, A. M. The embryonic development of the cortical plate in reptiles: a comparative study in Emys orbicularis and Lacerta agilis. J. Comp. Neurol. 215, 437–452 (1983).

    CAS  PubMed  Google Scholar 

  75. Luskin, M. B., Parnavelas, J. G. & Barfield, J. A. Neurons, astrocytes, and oligodendrocytes of the rat cerebral cortex originate from separate progenitor cells: an ultrastructural analysis of clonally related cells. J. Neurosci. 13, 1730–1750 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  76. Anderson, S. A., Eisenstat, D. D., Shi, L. & Rubenstein, J. L. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278, 474–476 (1997).

    CAS  PubMed  Google Scholar 

  77. Lavdas, A. A., Grigoriou, M., Pachnis, V. & Parnavelas, J. G. The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J. Neurosci. 19, 7881–7888 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Wichterle, H., Garcia-Verdugo, J. M., Herrera, D. G. & Alvarez-Buylla, A. Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nature Neurosci. 2, 461–466 (1999).

    CAS  PubMed  Google Scholar 

  79. Sussel, L., Marin, O., Kimura, S. & Rubenstein, J. L. Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 126, 3359–3370 (1999).

    CAS  PubMed  Google Scholar 

  80. Yuan, W. et al. The mouse SLIT family: secreted ligands for ROBO expressed in patterns that suggest a role in morphogenesis and axon guidance. Dev. Biol. 212, 290–306 (1999).

    CAS  PubMed  Google Scholar 

  81. Zhu, Y., Li, H., Zhou, L., Wu, J. Y. & Rao, Y. Cellular and molecular guidance of GABAergic neuronal migration from an extracortical origin to the neocortex. Neuron 23, 473–485 (1999).

    CAS  PubMed  Google Scholar 

  82. Powell, E. M., Mars, W. M. & Levitt, P. Hepatocyte growth factor/scatter factor is a motogen for interneurons migrating from the ventral to dorsal telencephalon. Neuron 30, 79–89 (2001).

    CAS  PubMed  Google Scholar 

  83. Marin, O., Yaron, A., Bagri, A., Tessier-Lavigne, M. & Rubenstein, J. L. Sorting of striatal and cortical interneurons regulated by semaphorin–neuropilin interactions. Science 293, 872–875 (2001).

    CAS  PubMed  Google Scholar 

  84. Metin, C. & Godement, P. The ganglionic eminence may be an intermediate target for corticofugal and thalamocortical axons. J. Neurosci. 16, 3219–3235 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Rakic, P. Limits of neurogenesis in primates. Science 227, 1054–1056 (1985).

    CAS  PubMed  Google Scholar 

  86. Gray, G. E., Leber, S. M. & Sanes, J. R. Migratory patterns of clonally related cells in the developing central nervous system. Experientia 46, 929–940 (1990).

    CAS  PubMed  Google Scholar 

  87. Wolfer, D. P., Henehan-Beatty, A., Stoeckli, E. T., Sonderegger, P. & Lipp, H. P. Distribution of TAG-1/axonin-1 in fibre tracts and migratory streams of the developing mouse nervous system. J. Comp. Neurol. 345, 1–32 (1994).

    CAS  PubMed  Google Scholar 

  88. Denaxa, M., Chan, C. H., Schachner, M., Parnavelas, J. G. & Karagogeos, D. The adhesion molecule TAG-1 mediates the migration of cortical interneurons from the ganglionic eminence along the corticofugal fiber system. Development 128, 4635–4644 (2001).

    CAS  PubMed  Google Scholar 

  89. Miller, M. W. Cogeneration of retrogradely labeled corticocortical projection and GABA-immunoreactive local circuit neurons in cerebral cortex. Brain Res. 355, 187–192 (1985).

    CAS  PubMed  Google Scholar 

  90. Wichterle, H., Turnbull, D. H., Nery, S., Fishell, G. & Alvarez-Buylla, A. In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128, 3759–3771 (2001).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Research in our laboratory was supported by the Wellcome Trust.

Author information

Authors and Affiliations

  1. Department of Anatomy and Developmental Biology, University College London, Gower Street, London, WC1E 6BT, UK

    Bagirathy Nadarajah & John G. Parnavelas

Authors
  1. Bagirathy Nadarajah
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John G. Parnavelas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bagirathy Nadarajah.

Supplementary information

Different modes of neuronal migration in the developing cortex (from reference 17).

CP, cortical plate; IZ, intermediate zone; PZ, proliferative (or ventricular) zone. Arrows point to cell bodies.

Examples of glia-guided migration and somal translocation (from reference 31).

In the first movie, the arrowhead points to the tip of the leading process. CP, cortical plate; VZ, ventricular zone.

Ventricle-directed migration (from reference 17).

The small arrow points to the tip of the leading process of the cell as it rapidly advances towards the ventricular surface (bottom). The large arrow points to a growing trailing process that will later become the leading process as the cell changes direction and moves towards the pial surface. CP, cortical plate; IZ, intermediate zone; VZ, ventricular zone.

Related links

Related links

DATABASES

LocusLink

ApoER2

astrotactin

N-cadherin

β-catenin

Cdk5

Dab1

DCX

dynactin

dynein

ErbB2

ErbB3

ErbB4

FLN1

HGF

α3β1 integrin

β2 integrin

LIS1

neuregulins

neuropilin 1

neuropilin 2

Nude

NUDEL

p35

reelin

class 3 semaphorins

SLIT1

TAG-1

VLDLR

FURTHER INFORMATION

Encyclopedia of Life Sciences

cerebral cortex development

Glossary

CAJAL–RETZIUS CELL

A transient pioneer neuron that is located in layer I of the developing neocortex and hippocampus.

X-INACTIVATED MOSAICS

Based on the process of X-linked gene inactivation, the analysis of X-linked transgenic markers (for example, LacZ) provides a method to distinguish between clonally related cell populations in the developing brain.

GOLGI STAINING

A histological staining technique that involves impregnating the tissue with silver nitrate. This labels a random subset of neurons, allowing the entire cell and its processes to be visualized.

REELER

A mutant mouse with a phenotype that is characterized by tremors, dystonia and ataxia.

DiI

A lipophilic carbocyanine dye that emits an intense fluorescence when incorporated into cell membranes. It is commonly used to track cell migration, or for the retrograde or anterograde tracing of axons. It can be used on both live and fixed tissue.

RHO GTPASE

A Ras-related GTPase that is involved in controlling the polymerization of actin.

DYNEIN MOTOR

A microtubule-based molecular motor that moves towards the minus end of microtubules.

LISSENCEPHALY

Literally meaning 'smooth brain', lissencephaly is a human brain disorder that is characterized by absence or reduction of the cerebral convolutions.

MILLER–DIEKER SYNDROME

A form of lissencephaly that is accompanied by dysmorphic facial features.

CALRETININ

A calcium-binding protein that is used as a marker of preplate neurons.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nadarajah, B., Parnavelas, J. Modes of neuronal migration in the developing cerebral cortex. Nat Rev Neurosci 3, 423–432 (2002). https://doi.org/10.1038/nrn845

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrn845

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing