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:

Neuronal migration in the adult brain: are we there yet?

Nature Reviews Neuroscience volume 8, pages 141–151 (2007)Cite this article

Key Points

  • In mammals, neurogenesis and neuronal migration continue into adulthood in restricted brain regions, such as the hippocampus and rostral migratory stream of the olfactory bulb.

  • The initiation of neuronal migration is regulated by a combination of motogenic, chemoattractive and chemorepulsive cues. Neuroblasts migrate as chains, sliding along each other.

  • New neurons in the mature brain polarize and extend a leading process in the direction of migration. Once the leading process has been stabilized, the nucleus is translocated towards it. Finally, nuclear translocation is arrested and the trailing process of the neuron is retracted towards the new position of the cell soma. Repetition of these three stages is a fundamental characteristic of neuronal migration in the mature brain.

  • Adult neuronal migration in the olfactory bulb might subserve a demand for continuous remodelling of the local neural circuitry, engendered by olfactory receptor turnover. In the hippocampus, the survival and incorporation of new neurons is activity dependent.

  • As animals age, the number of new neurons decreases. Morphological and functional differences between neurons generated at different times in the mature brain seem to parallel the general reduction of molecular cues that regulate neurogenesis and migration in the postnatal brain.

  • Limited, localized neuronal injury and hypoxia induce neurogenesis and replacement of neurons in the adult cerebral cortex. During tumorigenesis transformed tumour cells can migrate long distances in the adult human brain.

  • Evidence for organized, long-distance migration of newly generated neurons in the adult human brain is lacking. However, localized, short-distance migration within specific niches or migration as isolated neurons may occur. Understanding the mechanisms that can trigger and facilitate the recruitment and placement of correct numbers and types of neurons to where they are needed in the adult brain could be helpful in promoting functional recovery after brain injuries.

Abstract

The generation and targeting of appropriate numbers and types of neurons to where they are needed in the brain is essential for the establishment, maintenance and modification of neural circuitry. This review aims to summarize the patterns, mechanisms and functional significance of neuronal migration in the postnatal brain, with an emphasis on the migratory events that persist in the mature brain.

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: Radial and tangential migration of neurons in the developing cortex.
Figure 2: Neuronal migration in the postnatal and adult brain.
Figure 3: Initiation of neuronal migration.
Figure 4: Maintenance of neuronal migration.
Figure 5: Characteristic migratory behaviour of neuroblasts.
Figure 6: Neuronal polarity of migrating neurons of the adult brain.
Figure 7: Termination of neuronal migration.

Similar content being viewed by others

References

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

    Article  CAS  PubMed  Google Scholar 

  2. Mochida, G. H. & Walsh, C. A. Genetic basis of developmental malformations of the cerebral cortex. Arch. Neurol. 61, 637–640 (2004).

    Article  PubMed  Google Scholar 

  3. Nadarajah, B. & Parnavelas, J. G. Modes of neuronal migration in the developing cerebral cortex. Nature Rev. Neurosci. 3, 423–432 (2002).

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  5. 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).

    Article  CAS  PubMed  Google Scholar 

  6. Nadarajah, B. Radial glia and somal translocation of radial neurons in the developing cerebral cortex. Glia 43, 33–36 (2003).

    Article  PubMed  Google Scholar 

  7. 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).

    Article  CAS  PubMed  Google Scholar 

  8. De Carlos, J. A., Lopez-Mascaraque, L. & Valverde, F. Dynamics of cell migration from the lateral ganglionic eminence in the rat. J. Neurosci. 16, 6146–6156 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Marin, O. & Rubenstein, J. L. Cell migration in the forebrain. Annu. Rev. Neurosci. 26, 441–483 (2003). Together with references 1–6, this provides a thorough review of neuronal migration during embryonic development.

    Article  CAS  PubMed  Google Scholar 

  10. 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). Revealed evidence supporting the idea that GABA-containing interneurons migrate tangentially from the subpallium to the pallidum and the dependence of this process on Dlx transcription factors.

    Article  CAS  PubMed  Google Scholar 

  11. Bystron, I., Rakic, P., Molnar, Z. & Blakemore, C. The first neurons of the human cerebral cortex. Nature Neurosci. 9, 880–886 (2006).

    Article  CAS  PubMed  Google Scholar 

  12. Meyer, G., Soria, J. M., Martinez-Galan, J. R., Martin-Clemente, B. & Fairen, A. Different origins and developmental histories of transient neurons in the marginal zone of the fetal and neonatal rat cortex. J. Comp. Neurol. 397, 493–518 (1998).

    Article  CAS  PubMed  Google Scholar 

  13. Polleux, F., Whitford, K. L., Dijkhuizen, P. A., Vitalis, T. & Ghosh, A. Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling. Development 129, 3147–3160 (2002).

    CAS  PubMed  Google Scholar 

  14. Komuro, H. & Rakic, P. Dynamics of granule cell migration: a confocal microscopic study in acute cerebellar slice preparations. J. Neurosci. 15, 1110–1120 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. 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).

    Article  CAS  PubMed  Google Scholar 

  16. Ramón y Cajal, S. Degeneration and Regeneration of the Nervous System (Oxford Univ. Press/Humphrey Milford, London, 1928).

    Google Scholar 

  17. Bhardwaj, R. D. et al. Neocortical neurogenesis in humans is restricted to development. Proc. Natl Acad. Sci. USA 103, 12564–12568 (2006). Establishes that no newborn neurons are present in the adult human neocortex.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Mizrahi, A. & Katz, L. C. Dendritic stability in the adult olfactory bulb. Nature Neurosci. 6, 1201–1207 (2003).

    Article  CAS  PubMed  Google Scholar 

  19. Kornack, D. R. & Rakic, P. Cell proliferation without neurogenesis in adult primate neocortex. Science 294, 2127–2130 (2001).

    Article  CAS  PubMed  Google Scholar 

  20. Altman, J. & Das, G. D. Autoradiographic and histological studies of postnatal neurogenesis. I. A longitudinal investigation of the kinetics, migration and transformation of cells incorporating tritiated thymidine in neonate rats, with special reference to postnatal neurogenesis in some brain regions. J. Comp. Neurol. 126, 337–389 (1966).

    Article  CAS  PubMed  Google Scholar 

  21. Bayer, S. A. 3H-thymidine-radiographic studies of neurogenesis in the rat olfactory bulb. Exp. Brain Res. 50, 329–340 (1983).

    CAS  PubMed  Google Scholar 

  22. Kaplan, M. S. & Bell, D. H. Neuronal proliferation in the 9-month-old rodent — radioautographic study of granule cells in the hippocampus. Exp. Brain Res. 52, 1–5 (1983).

    Article  CAS  PubMed  Google Scholar 

  23. Levison, S. W., Chuang, C., Abramson, B. J. & Goldman, J. E. The migrational patterns and developmental fates of glial precursors in the rat subventricular zone are temporally regulated. Development 119, 611–622 (1993).

    CAS  PubMed  Google Scholar 

  24. Lois, C. & Alvarez-Buylla, A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl Acad. Sci. USA 90, 2074–2077 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Luskin, M. B. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11, 173–189 (1993).

    Article  CAS  PubMed  Google Scholar 

  26. Taupin, P. & Gage, F. H. Adult neurogenesis and neural stem cells of the central nervous system in mammals. J. Neurosci. Res. 69, 745–749 (2002).

    Article  CAS  PubMed  Google Scholar 

  27. Schmahmann, J. D. Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. J. Neuropsychiatry Clin. Neurosci. 16, 367–378 (2004).

    Article  PubMed  Google Scholar 

  28. Wang, V. Y. & Zoghbi, H. Y. Genetic regulation of cerebellar development. Nature Rev. Neurosci. 2, 484–491 (2001).

    Article  CAS  Google Scholar 

  29. Friede, R. L. Dating the development of human cerebellum. Acta Neuropathol. (Berl.) 23, 48–58 (1973).

    Article  CAS  Google Scholar 

  30. Solecki, D. J., Govek, E. E. & Hatten, M. E. mPar6α controls neuronal migration. J. Neurosci. 26, 10624–10625 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Machold, R. & Fishell, G. Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron 48, 17–24 (2005).

    Article  CAS  PubMed  Google Scholar 

  32. Wang, V. Y., Rose, M. F. & Zoghbi, H. Y. Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron 48, 31–43 (2005).

    Article  CAS  PubMed  Google Scholar 

  33. Gilthorpe, J. D., Papantoniou, E. K., Chedotal, A., Lumsden, A. & Wingate, R. J. The migration of cerebellar rhombic lip derivatives. Development 129, 4719–4728 (2002).

    CAS  PubMed  Google Scholar 

  34. Solecki, D. J., Govek, E. E., Tomoda, T. & Hatten, M. E. Neuronal polarity in CNS development. Genes Dev. 20, 2639–2647 (2006). Outlines recent advances in our understanding of neuronal polarity and its relevance to developmental events, including neuronal migration.

    Article  CAS  PubMed  Google Scholar 

  35. Komuro, H. & Kumada, T. Ca2+ transients control CNS neuronal migration. Cell Calcium 37, 387–393 (2005).

    Article  CAS  PubMed  Google Scholar 

  36. Sisk, C. L. & Foster, D. L. The neural basis of puberty and adolescence. Nature Neurosci. 7, 1040–1047 (2004).

    Article  CAS  PubMed  Google Scholar 

  37. Schwanzel-Fukuda, M. & Pfaff, D. W. Origin of luteinizing hormone-releasing hormone neurons. Nature 338, 161–164 (1989).

    Article  CAS  PubMed  Google Scholar 

  38. Tobet, S. A. & Schwarting, G. A. Minireview: recent progress in gonadotropin-releasing hormone neuronal migration. Endocrinology 147, 1159–1165 (2006).

    Article  CAS  PubMed  Google Scholar 

  39. Wierman, M. E. et al. Molecular mechanisms of gonadotropin-releasing hormone neuronal migration. Trends Endocrinol. Metab. 15, 96–102 (2004).

    Article  CAS  PubMed  Google Scholar 

  40. Cariboni, A. & Maggi, R. Kallmann's syndrome, a neuronal migration defect. Cell. Mol. Life Sci. 63, 2512–2526 (2006).

    Article  CAS  PubMed  Google Scholar 

  41. Eichenbaum, H. Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron 44, 109–120 (2004).

    Article  CAS  PubMed  Google Scholar 

  42. Stanfield, B. B. & Cowan, W. M. The development of the hippocampus and dentate gyrus in normal and reeler mice. J. Comp. Neurol. 185, 423–459 (1979).

    Article  CAS  PubMed  Google Scholar 

  43. Forster, E. et al. Reelin, Disabled 1, and β1 integrins are required for the formation of the radial glial scaffold in the hippocampus. Proc. Natl Acad. Sci. USA 99, 13178–13183 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Weiss, K. H. et al. Malformation of the radial glial scaffold in the dentate gyrus of reeler mice, scrambler mice, and ApoER2/VLDLR-deficient mice. J. Comp. Neurol. 460, 56–65 (2003).

    Article  CAS  PubMed  Google Scholar 

  45. Zhao, S., Chai, X., Forster, E. & Frotscher, M. Reelin is a positional signal for the lamination of dentate granule cells. Development 131, 5117–5125 (2004).

    Article  CAS  PubMed  Google Scholar 

  46. Morozov, Y. M., Ayoub, A. E. & Rakic, P. Translocation of synaptically connected interneurons across the dentate gyrus of the early postnatal rat hippocampus. J. Neurosci. 26, 5017–5027 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. 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).

    Article  CAS  PubMed  Google Scholar 

  48. Luzzati, F. et al. Glia-independent chains of neuroblasts through the subcortical parenchyma of the adult rabbit brain. Proc. Natl Acad. Sci. USA 100, 13036–13041 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Kornack, D. R. & Rakic, P. Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc. Natl Acad. Sci. USA 96, 5768–5773 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Sanai, N. et al. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427, 740–744 (2004). Demonstrates that there is no RMS indicative of organized, long-distance neuronal migration in the adult human brain. This paper, together with references 161–163, also shows the presence of neural stem cells in the adult human brain.

    Article  CAS  PubMed  Google Scholar 

  51. Lois, C. & Alvarez-Buylla, A. Long-distance neuronal migration in the adult mammalian brain. Science 264, 1145–1148 (1994). Together with reference 25, this demonstrates how long-distance migration of new neurons occurs in the adult mammalian brain.

    Article  CAS  PubMed  Google Scholar 

  52. Mason, H. A., Ito, S. & Corfas, G. Extracellular signals that regulate the tangential migration of olfactory bulb neuronal precursors: inducers, inhibitors, and repellents. J. Neurosci. 21, 7654–7663 (2001). Identified a novel, astroglial-derived migration inducing factor (MIA) for RMS neuroblasts.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Murase, S. & Horwitz, A. F. Deleted in colorectal carcinoma and differentially expressed integrins mediate the directional migration of neural precursors in the rostral migratory stream. J. Neurosci. 22, 3568–3579 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Liu, G. & Rao, Y. Neuronal migration from the forebrain to the olfactory bulb requires a new attractant persistent in the olfactory bulb. J. Neurosci. 23, 6651–6659 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Wu, W. et al. Directional guidance of neuronal migration in the olfactory system by the protein Slit. Nature 400, 331–336 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Kirschenbaum, B., Doetsch, F., Lois, C. & Alvarez-Buylla, A. Adult subventricular zone neuronal precursors continue to proliferate and migrate in the absence of the olfactory bulb. J. Neurosci. 19, 2171–2180 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Jankovski, A. & Sotelo, C. Subventricular zone–olfactory bulb migratory pathway in the adult mouse: cellular composition and specificity as determined by heterochronic and heterotopic transplantation. J. Comp. Neurol. 371, 376–396 (1996).

    Article  CAS  PubMed  Google Scholar 

  58. Lois, C., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Chain migration of neuronal precursors. Science 271, 978–981 (1996).

    Article  CAS  PubMed  Google Scholar 

  59. Wichterle, H., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Direct evidence for homotypic, glia-independent neuronal migration. Neuron 18, 779–791 (1997). Describes the migratory organization and dynamics of new neurons generated in the SVZ.

    Article  CAS  PubMed  Google Scholar 

  60. Lim, D. A. & Alvarez-Buylla, A. Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. Proc. Natl Acad. Sci. USA 96, 7526–7531 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Menezes, J. R., Smith, C. M., Nelson, K. C. & Luskin, M. B. The division of neuronal progenitor cells during migration in the neonatal mammalian forebrain. Mol. Cell. Neurosci. 6, 496–508 (1995).

    Article  CAS  PubMed  Google Scholar 

  62. Doetsch, F., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 17, 5046–5061 (1997). Characterizes the complex cellular organization of the adult SVZ.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Doetsch, F., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Regeneration of a germinal layer in the adult mammalian brain. Proc. Natl Acad. Sci. USA 96, 11619–11624 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Doetsch, F., Caille, I., Lim, D. A., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703–716 (1999).

    Article  CAS  PubMed  Google Scholar 

  65. Capela, A. & Temple, S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 35, 865–875 (2002).

    Article  PubMed  Google Scholar 

  66. Morshead, C. M., Garcia, A. D., Sofroniew, M. V. & van der Kooy, D. The ablation of glial fibrillary acidic protein-positive cells from the adult central nervous system results in the loss of forebrain neural stem cells but not retinal stem cells. Eur. J. Neurosci. 18, 76–84 (2003).

    Article  PubMed  Google Scholar 

  67. Ghashghaei, H. T. et al. The role of neuregulin–ErbB4 interactions on the proliferation and organization of cells in the subventricular zone. Proc. Natl Acad. Sci. USA 103, 1930–1935 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Marillat, V. et al. Spatiotemporal expression patterns of slit and robo genes in the rat brain. J. Comp. Neurol. 442, 130–155 (2002).

    Article  PubMed  Google Scholar 

  69. Nguyen-Ba-Charvet, K. T. et al. Multiple roles for Slits in the control of cell migration in the rostral migratory stream. J. Neurosci. 24, 1497–1506 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Sawamoto, K. et al. New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 311, 629–632 (2006). Shows how the activity of ependymal cell cilia in the lateral ventricles may convey gradients of migration-influencing cues to newly generated neuroblasts in the SVZ.

    Article  CAS  PubMed  Google Scholar 

  71. Higginbotham, H., Tanaka, T., Brinkman, B. C. & Gleeson, J. G. GSK3β and PKCζ function in centrosome localization and process stabilization during Slit-mediated neuronal repolarization. Mol. Cell. Neurosci. 32, 118–132 (2006).

    Article  CAS  PubMed  Google Scholar 

  72. Marin, O. et al. Directional guidance of interneuron migration to the cerebral cortex relies on subcortical Slit1/2-independent repulsion and cortical attraction. Development 130, 1889–1901 (2003).

    Article  CAS  PubMed  Google Scholar 

  73. Hu, H. Chemorepulsion of neuronal migration by Slit2 in the developing mammalian forebrain. Neuron 23, 703–711 (1999).

    Article  CAS  PubMed  Google Scholar 

  74. Hu, H. Cell-surface heparan sulfate is involved in the repulsive guidance activities of Slit2 protein. Nature Neurosci. 4, 695–701 (2001).

    Article  CAS  PubMed  Google Scholar 

  75. Juliano, R. L. Signal transduction by cell adhesion receptors and the cytoskeleton: functions of integrins, cadherins, selectins, and immunoglobulin-superfamily members. Annu. Rev. Pharmacol. Toxicol. 42, 283–323 (2002).

    Article  CAS  PubMed  Google Scholar 

  76. Tomasiewicz, H. et al. Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system. Neuron 11, 1163–1174 (1993).

    Article  CAS  PubMed  Google Scholar 

  77. Cremer, H. et al. Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367, 455–459 (1994).

    Article  CAS  PubMed  Google Scholar 

  78. Ono, K., Tomasiewicz, H., Magnuson, T. & Rutishauser, U. N-CAM mutation inhibits tangential neuronal migration and is phenocopied by enzymatic removal of polysialic acid. Neuron 13, 595–609 (1994). Demonstrates that NCAM and polysialation of NCAM are essential for neuroblast chain migration in the RMS.

    Article  CAS  PubMed  Google Scholar 

  79. Hu, H. Polysialic acid regulates chain formation by migrating olfactory interneuron precursors. J. Neurosci. Res. 61, 480–492 (2000).

    Article  CAS  PubMed  Google Scholar 

  80. Hu, H., Tomasiewicz, H., Magnuson, T. & Rutishauser, U. The role of polysialic acid in migration of olfactory bulb interneuron precursors in the subventricular zone. Neuron 16, 735–743 (1996).

    Article  CAS  PubMed  Google Scholar 

  81. Murase, S. & Horwitz, A. F. Directions in cell migration along the rostral migratory stream: the pathway for migration in the brain. Curr. Top. Dev. Biol. 61, 135–152 (2004).

    Article  CAS  PubMed  Google Scholar 

  82. Chazal, G., Durbec, P., Jankovski, A., Rougon, G. & Cremer, H. Consequences of neural cell adhesion molecule deficiency on cell migration in the rostral migratory stream of the mouse. J. Neurosci. 20, 1446–1457 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Anton, E. S. et al. Receptor tyrosine kinase ErbB4 modulates neuroblast migration and placement in the adult forebrain. Nature Neurosci. 7, 1319–1328 (2004). Demonstrates how neuregulin–ErbB4 signalling regulates neuroblast migration in the RMS.

    Article  CAS  PubMed  Google Scholar 

  84. Conover, J. C. et al. Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone. Nature Neurosci. 3, 1091–1097 (2000).

    Article  CAS  PubMed  Google Scholar 

  85. Jacques, T. S. et al. Neural precursor cell chain migration and division are regulated through different β1 integrins. Development 125, 3167–3177 (1998).

    CAS  PubMed  Google Scholar 

  86. Emsley, J. G. & Hagg, T. α6β1 integrin directs migration of neuronal precursors in adult mouse forebrain. Exp. Neurol. 183, 273–285 (2003).

    Article  CAS  PubMed  Google Scholar 

  87. Schmid, R. S., Jo, R., Shelton, S., Kreidberg, J. A. & Anton, E. S. Reelin, integrin and DAB1 interactions during embryonic cerebral cortical development. Cereb. Cortex 15, 1632–1636 (2005).

    Article  PubMed  Google Scholar 

  88. Gates, M. A. et al. Cell and molecular analysis of the developing and adult mouse subventricular zone of the cerebral hemispheres. J. Comp. Neurol. 361, 249–266 (1995).

    Article  CAS  PubMed  Google Scholar 

  89. Thomas, L. B., Gates, M. A. & Steindler, D. A. Young neurons from the adult subependymal zone proliferate and migrate along an astrocyte, extracellular matrix-rich pathway. Glia 17, 1–14 (1996).

    Article  CAS  PubMed  Google Scholar 

  90. de Chevigny, A. et al. Delayed onset of odor detection in neonatal mice lacking tenascin-C. Mol. Cell. Neurosci. 32, 174–186 (2006).

    Article  CAS  PubMed  Google Scholar 

  91. Kiernan, B. W., Gotz, B., Faissner, A. & ffrench-Constant, C. Tenascin-C inhibits oligodendrocyte precursor cell migration by both adhesion-dependent and adhesion-independent mechanisms. Mol. Cell. Neurosci. 7, 322–335 (1996).

    Article  CAS  PubMed  Google Scholar 

  92. Saga, Y., Yagi, T., Ikawa, Y., Sakakura, T. & Aizawa, S. Mice develop normally without tenascin. Genes Dev. 6, 1821–1831 (1992).

    Article  CAS  PubMed  Google Scholar 

  93. Colognato, H. et al. CNS integrins switch growth factor signalling to promote target-dependent survival. Nature Cell Biol. 4, 833–841 (2002).

    Article  CAS  PubMed  Google Scholar 

  94. Davy, A. & Robbins, S. M. Ephrin-A5 modulates cell adhesion and morphology in an integrin-dependent manner. EMBO J. 19, 5396–5405 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Prevost, N. et al. Eph kinases and ephrins support thrombus growth and stability by regulating integrin outside-in signaling in platelets. Proc. Natl Acad. Sci. USA 102, 9820–9825 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Koshida, S. et al. Integrinα5-dependent fibronectin accumulation for maintenance of somite boundaries in zebrafish embryos. Dev. Cell 8, 587–598 (2005).

    Article  CAS  PubMed  Google Scholar 

  97. de Anda, F. C. et al. Centrosome localization determines neuronal polarity. Nature 436, 704–708 (2005).

    Article  CAS  PubMed  Google Scholar 

  98. Tsai, L. H. & Gleeson, J. G. Nucleokinesis in neuronal migration. Neuron 46, 383–388 (2005).

    Article  CAS  PubMed  Google Scholar 

  99. Solecki, D. J., Model, L., Gaetz, J., Kapoor, T. M. & Hatten, M. E. Par6α signaling controls glial-guided neuronal migration. Nature Neurosci. 7, 1195–1203 (2004).

    Article  PubMed  Google Scholar 

  100. Koizumi, H. et al. Doublecortin maintains bipolar shape and nuclear translocation during migration in the adult forebrain. Nature Neurosci. 9, 779–786 (2006). Shows that doublecortin is crucial for the nuclear translocation and migratory morphology of new neurons in the adult brain.

    Article  CAS  PubMed  Google Scholar 

  101. Kappeler, C. et al. Branching and nucleokinesis defects in migrating interneurons derived from doublecortin knockout mice. Hum. Mol. Genet. 15, 1387–1400 (2006).

    Article  CAS  PubMed  Google Scholar 

  102. Yoshihara, S., Omichi, K., Yanazawa, M., Kitamura, K. & Yoshihara, Y. Arx homeobox gene is essential for development of mouse olfactory system. Development 132, 751–762 (2005).

    Article  CAS  PubMed  Google Scholar 

  103. D'Arcangelo, G. et al. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374, 719–723 (1995).

    Article  CAS  PubMed  Google Scholar 

  104. Rakic, P. & Sidman, R. L. Sequence of developmental abnormalities leading to granule cell deficit in cerebellar cortex of weaver mutant mice. J. Comp. Neurol. 152, 103–132 (1973).

    Article  CAS  PubMed  Google Scholar 

  105. Hack, I., Bancila, M., Loulier, K., Carroll, P. & Cremer, H. Reelin is a detachment signal in tangential chain-migration during postnatal neurogenesis. Nature Neurosci. 5, 939–945 (2002). Describes how reelin might function to end the migration of new neurons when they reach their target in the olfactory bulb.

    Article  CAS  PubMed  Google Scholar 

  106. Saghatelyan, A., de Chevigny, A., Schachner, M. & Lledo, P. M. Tenascin-R mediates activity-dependent recruitment of neuroblasts in the adult mouse forebrain. Nature Neurosci. 7, 347–356 (2004).

    Article  CAS  PubMed  Google Scholar 

  107. 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).

    Article  CAS  PubMed  Google Scholar 

  108. Pozas, E. & Ibanez, C. F. GDNF and GFRα1 promote differentiation and tangential migration of cortical GABAergic neurons. Neuron 45, 701–713 (2005).

    Article  CAS  PubMed  Google Scholar 

  109. 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).

    Article  CAS  PubMed  Google Scholar 

  110. Andrews, W. et al. Robo1 regulates the development of major axon tracts and interneuron migration in the forebrain. Development 133, 2243–2252 (2006).

    Article  CAS  PubMed  Google Scholar 

  111. Magavi, S. S., Leavitt, B. R. & Macklis, J. D. Induction of neurogenesis in the neocortex of adult mice. Nature 405, 951–955 (2000).

    Article  CAS  PubMed  Google Scholar 

  112. Nakatomi, H. et al. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110, 429–441 (2002).

    Article  CAS  PubMed  Google Scholar 

  113. Van Praag, H. et al. Functional neurogenesis in the adult hippocampus. Nature 415, 1030–1034 (2002).

    Article  CAS  PubMed  Google Scholar 

  114. Yokoi, M., Mori, K. & Nakanishi, S. Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc. Natl Acad. Sci. USA 92, 3371–3375 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Mori, K., Nagao, H. & Yoshihara, Y. The olfactory bulb: coding and processing of odor molecule information. Science 286, 711–715 (1999).

    Article  CAS  PubMed  Google Scholar 

  116. Magavi, S. S., Mitchell, B. D., Szentirmai, O., Carter, B. S. & Macklis, J. D. Adult-born and preexisting olfactory granule neurons undergo distinct experience-dependent modifications of their olfactory responses in vivo. J. Neurosci. 25, 10729–10739 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Nilsson, M., Perfilieva, E., Johansson, U., Orwar, O. & Eriksson, P. S. Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J. Neurobiol. 39, 569–578 (1999).

    Article  CAS  PubMed  Google Scholar 

  118. Shors, T. J. et al. Neurogenesis in the adult is involved in the formation of trace memories. Nature 410, 372–376 (2001).

    Article  CAS  PubMed  Google Scholar 

  119. Rochefort, C., Gheusi, G., Vincent, J. D. & Lledo, P. M. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J. Neurosci. 22, 2679–2689 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Gheusi, G. et al. Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc. Natl Acad. Sci. USA 97, 1823–1828 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Enwere, E. et al. Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J. Neurosci. 24, 8354–8365 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  122. Cecchi, G. A., Petreanu, L. T., Alvarez-Buylla, A. & Magnasco, M. O. Unsupervised learning and adaptation in a model of adult neurogenesis. J. Comput. Neurosci. 11, 175–182 (2001).

    Article  CAS  PubMed  Google Scholar 

  123. Bolteus, A. J. & Bordey, A. GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J. Neurosci. 24, 7623–7631 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Carleton, A., Petreanu, L. T., Lansford, R., Alvarez-Buylla, A. & Lledo, P. M. Becoming a new neuron in the adult olfactory bulb. Nature Neurosci. 6, 507–518 (2003). Describes the physiological properties of adult-born olfactory bulb interneurons at various stages of maturation in adult mice.

    Article  CAS  PubMed  Google Scholar 

  125. Tashiro, A., Sandler, V. M., Toni, N., Zhao, C. & Gage, F. H. NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature 442, 929–933 (2006).

    Article  CAS  PubMed  Google Scholar 

  126. Aimone, J. B., Wiles, J. & Gage, F. H. Potential role for adult neurogenesis in the encoding of time in new memories. Nature Neurosci. 9, 723–727 (2006).

    Article  CAS  PubMed  Google Scholar 

  127. Gould, E., Beylin, A., Tanapat, P., Reeves, A. & Shors, T. J. Learning enhances adult neurogenesis in the hippocampal formation. Nature Neurosci. 2, 260–265 (1999).

    Article  CAS  PubMed  Google Scholar 

  128. Dayer, A. G., Cleaver, K. M., Abouantoun, T. & Cameron, H. A. New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors. J. Cell Biol. 168, 415–427 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Kaplan, M. S. Neurogenesis in the 3-month-old rat visual cortex. J. Comp. Neurol. 195, 323–338 (1981).

    Article  CAS  PubMed  Google Scholar 

  130. Koketsu, D., Mikami, A., Miyamoto, Y. & Hisatsune, T. Nonrenewal of neurons in the cerebral neocortex of adult macaque monkeys. J. Neurosci. 23, 937–942 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Spalding, K. L., Bhardwaj, R. D., Buchholz, B. A., Druid, H. & Frisen, J. Retrospective birth dating of cells in humans. Cell 122, 133–143 (2005).

    Article  CAS  PubMed  Google Scholar 

  132. Kokoeva, M. V., Yin, H. & Flier, J. S. Neurogenesis in the hypothalamus of adult mice: potential role in energy balance. Science 310, 679–683 (2005).

    Article  CAS  PubMed  Google Scholar 

  133. Luo, J., Daniels, S. B., Lennington, J. B., Notti, R. Q. & Conover, J. C. The aging neurogenic subventricular zone. Aging Cell 5, 139–152 (2006).

    Article  CAS  PubMed  Google Scholar 

  134. Mirich, J. M., Williams, N. C., Berlau, D. J. & Brunjes, P. C. Comparative study of aging in the mouse olfactory bulb. J. Comp. Neurol. 454, 361–372 (2002).

    Article  PubMed  Google Scholar 

  135. Pencea, V., Bingaman, K. D., Freedman, L. J. & Luskin, M. B. Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp. Neurol. 172, 1–16 (2001).

    Article  CAS  PubMed  Google Scholar 

  136. Lemasson, M., Saghatelyan, A., Olivo-Marin, J. C. & Lledo, P. M. Neonatal and adult neurogenesis provide two distinct populations of newborn neurons to the mouse olfactory bulb. J. Neurosci. 25, 6816–6825 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Caporaso, G. L., Lim, D. A., Alvarez-Buylla, A. & Chao, M. V. Telomerase activity in the subventricular zone of adult mice. Mol. Cell. Neurosci. 23, 693–702 (2003).

    Article  CAS  PubMed  Google Scholar 

  138. Lichtenwalner, R. J. & Parent, J. M. Adult neurogenesis and the ischemic forebrain. J. Cereb. Blood Flow Metab. 26, 1–20 (2006).

    Article  CAS  PubMed  Google Scholar 

  139. Fallon, J. et al. In vivo induction of massive proliferation, directed migration, and differentiation of neural cells in the adult mammalian brain. Proc. Natl Acad. Sci. USA 97, 14686–14691 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Houle, J. D. et al. Combining an autologous peripheral nervous system 'bridge' and matrix modification by chondroitinase allows robust, functional regeneration beyond a hemisection lesion of the adult rat spinal cord. J. Neurosci. 26, 7405–7415 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Johansson, B. B. Environmental influence on recovery after brain lesions — experimental and clinical data. J. Rehabil. Med. 11–16 (2003).

  142. Raisman, G. Myelin inhibitors: does NO mean GO? Nature Rev. Neurosci. 5, 157–161 (2004).

    Article  CAS  Google Scholar 

  143. Kozlova, E. N. Differentiation and migration of astrocytes in the spinal cord following dorsal root injury in the adult rat. Eur. J. Neurosci. 17, 782–790 (2003).

    Article  PubMed  Google Scholar 

  144. Lee, S. R. et al. Involvement of matrix metalloproteinase in neuroblast cell migration from the subventricular zone after stroke. J. Neurosci. 26, 3491–3495 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Sundholm-Peters, N. L., Yang, H. K., Goings, G. E., Walker, A. S. & Szele, F. G. Subventricular zone neuroblasts emigrate toward cortical lesions. J. Neuropathol. Exp. Neurol. 64, 1089–1100 (2005).

    Article  PubMed  Google Scholar 

  146. Stefansson, H. et al. Neuregulin 1 and susceptibility to schizophrenia. Am. J. Hum. Genet. 71, 877–892 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  147. Stefansson, H., Thorgeirsson, T. E., Gulcher, J. R. & Stefansson, K. Neuregulin 1 in schizophrenia: out of Iceland. Mol. Psychiatry 8, 639–640 (2003).

    Article  CAS  PubMed  Google Scholar 

  148. Yang, J. Z. et al. Association study of neuregulin 1 gene with schizophrenia. Mol. Psychiatry 8, 706–709 (2003).

    Article  CAS  PubMed  Google Scholar 

  149. Norton, N. et al. Evidence that interaction between neuregulin 1 and its receptor erbB4 increases susceptibility to schizophrenia. Am. J. Med. Genet. B Neuropsychiatr. Genet. 141, 96–101 (2006).

    Article  CAS  Google Scholar 

  150. Hahn, C. G. et al. Altered neuregulin 1–erbB4 signaling contributes to NMDA receptor hypofunction in schizophrenia. Nature Med. 12, 824–828 (2006).

    Article  CAS  PubMed  Google Scholar 

  151. Ishizuka, K., Paek, M., Kamiya, A. & Sawa, A. A review of disrupted-in-schizophrenia-1 (DISC1): neurodevelopment, cognition, and mental conditions. Biol. Psychiatry 59, 1189–1197 (2006).

    Article  CAS  PubMed  Google Scholar 

  152. Eastwood, S. L. & Harrison, P. J. Cellular basis of reduced cortical reelin expression in schizophrenia. Am. J. Psychiatry 163, 540–542 (2006).

    Article  PubMed  Google Scholar 

  153. Fatemi, S. H. Reelin glycoprotein in autism and schizophrenia. Int. Rev. Neurobiol. 71, 179–187 (2005).

    Article  CAS  PubMed  Google Scholar 

  154. Tueting, P., Doueiri, M. S., Guidotti, A., Davis, J. M. & Costa, E. Reelin down-regulation in mice and psychosis endophenotypes. Neurosci. Biobehav. Rev. 30, 1065–1077 (2006).

    Article  CAS  PubMed  Google Scholar 

  155. Haas, C. A. et al. Role for reelin in the development of granule cell dispersion in temporal lobe epilepsy. J. Neurosci. 22, 5797–5802 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Encinas, J. M., Vaahtokari, A. & Enikolopov, G. Fluoxetine targets early progenitor cells in the adult brain. Proc. Natl Acad. Sci. USA 103, 8233–8238 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Dranovsky, A. & Hen, R. Hippocampal neurogenesis: regulation by stress and antidepressants. Biol. Psychiatry 59, 1136–1143 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Santarelli, L. et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301, 805–809 (2003).

    Article  CAS  PubMed  Google Scholar 

  159. Gould, E., Tanapat, P., McEwen, B. S., Flugge, G. & Fuchs, E. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc. Natl Acad. Sci. USA 95, 3168–3171 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Malberg, J. E., Eisch, A. J., Nestler, E. J. & Duman, R. S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 20, 9104–9110 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Palmer, T. D. et al. Cell culture. Progenitor cells from human brain after death. Nature 411, 42–43 (2001).

    Article  CAS  PubMed  Google Scholar 

  162. Nunes, M. C. et al. Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nature Med. 9, 439–447 (2003).

    Article  CAS  PubMed  Google Scholar 

  163. Eriksson, P. S. et al. Neurogenesis in the adult human hippocampus. Nature Med. 4, 1313–1317 (1998).

    Article  CAS  PubMed  Google Scholar 

  164. Bedard, A. & Parent, A. Evidence of newly generated neurons in the human olfactory bulb. Brain Res. Dev. Brain Res. 151, 159–168 (2004).

    Article  CAS  PubMed  Google Scholar 

  165. Liu, Z. & Martin, L. J. Olfactory bulb core is a rich source of neural progenitor and stem cells in adult rodent and human. J. Comp. Neurol. 459, 368–391 (2003).

    Article  PubMed  Google Scholar 

  166. Quinones-Hinojosa, A. et al. Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J. Comp. Neurol. 494, 415–434 (2006). Describes the unique cellular organization of the human SVZ.

    Article  PubMed  Google Scholar 

  167. Font, E., Desfilis, E., Perez-Canellas, M. M. & Garcia-Verdugo, J. M. Neurogenesis and neuronal regeneration in the adult reptilian brain. Brain Behav. Evol. 58, 276–295 (2001).

    Article  CAS  PubMed  Google Scholar 

  168. Grandel, H., Kaslin, J., Ganz, J., Wenzel, I. & Brand, M. Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate. Dev. Biol. 295, 263–277 (2006).

    Article  CAS  PubMed  Google Scholar 

  169. Martin, J. H. Neuroanatomy: Text and Atlas 2nd edn (Appleton & Lange, Stamford, Connecticut, 1996).

    Google Scholar 

  170. Morales, D. & Hatten, M. E. Molecular markers of neuronal progenitors in the embryonic cerebellar anlage. J. Neurosci. 26, 12226–12236 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Supported by grants from the National Institutes of Mental Health (NIMH), USA, and Staglin Music Festival Award (NARSAD), USA.

Author information

Authors and Affiliations

  1. UNC Neuroscience Center and the Department of Cell and Molecular Physiology, Room 7109B, 103 Mason Farm Road, The University of North Carolina School of Medicine, Chapel Hill, 27599-7250, North Carolina, USA

    H. Troy Ghashghaei & E. S. Anton

  2. Department of Molecular Biomedical Sciences, School of Veterinary Medicine, North Carolina State University, Raleigh, 27606, North Carolina, USA

    H. Troy Ghashghaei

  3. Molecular and Integrative Neuroscience Department, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, 92037, California, USA

    Cary Lai

Authors
  1. H. Troy Ghashghaei
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cary Lai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. S. Anton
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. S. Anton.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

FURTHER INFORMATION

Anton's laboratory

Glossary

Radial glial cells

Cells that span the radial axis of the developing cortex and serve as precursors or guides for newly born postmitotic neurons on their way into the mantle zone.

Ventricular zone

Also known as the proliferative zone, this is the part of the neuroepithelium that faces the ventricular (inner) surface of the neural tube, where cells are proliferating.

Cortical plate

The top of the developing cerebral cortex, where neurons end their migration and start to assemble into distinct neuronal layers.

Leading process

The process of a migrating neuron that is extended towards the direction of migration.

Ganglionic eminence

The part of the subpallium that gives rise to tangentially migrating interneurons.

Rostral migratory stream

Neural cells born in the subventricular zone migrate tangentially as cellular chains to the olfactory bulb. This organized stream of migrating neuroblasts forms the rostral migratory stream.

Subventricular zone

(SVZ). The mitotically active region immediately adjacent to the rostral lining of the lateral ventricles where neural stem cells and restricted progenitor cells reside.

Neuronal chains

Neuroblasts migrating in the rostral migratory stream slide along each other, forming interlinked chains of migrating neurons.

Glial tube

Neuroblasts in the rostral migratory stream migrate through tubes composed of astrocyte-like glial cells. These glial tubes might help to orient the migration of neuroblasts.

Matrigel

A solubulized extract of basement membrane proteins prepared from EHS mouse sarcoma cells.

Adhesion molecules

Families of cell-surface or secreted molecules that mediate cell–cell or cell–substrate adhesion.

Neurogenic niches

Sites in the nervous system where neural precursors proliferate and give rise to new neural cells.

Receptive fields

The area of the sensory space in which stimulus presentation leads to the response of a particular sensory neuron.

Transitory amplifying progenitor cell

Slow-dividing neural stem cells in the subventricular zone give rise to transitory amplifying progenitors (nestin+ and DLX2+), which, in turn, rapidly proliferate to give rise to neuroblasts migrating in the rostral migratory stream.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ghashghaei, H., Lai, C. & Anton, E. Neuronal migration in the adult brain: are we there yet?. Nat Rev Neurosci 8, 141–151 (2007). https://doi.org/10.1038/nrn2074

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrn2074

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