Laminating the hippocampus (original) (raw)

• 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
• Altman, J. & Das, G. D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 124, 319–335 (1965).
  CAS Google Scholar
• 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, 337–390 (1966).
  CAS PubMed Google Scholar
• Altman, J. Autoradiographic and histological studies of postnatal neurogenesis. II. A longitudinal investigation of the kinetics, migration and transformation of cells incorporating tritiated thymidine in infant rats, with special reference to postnatal neurogenesis in some brain regions. J. Comp. Neurol. 128, 431–474 (1966).
  Google Scholar
• Bayer, S. A. & Altman, J. Radiation-induced interference with postnatal hippocampal cytogenesis in rats and its long-term effects in the acquisition of neurons and glia. J. Comp. Neurol. 163, 1–20 (1975).
  Google Scholar
• Bayer, S. A. Development of the hippocampal region in the rat. I. Neurogenesis examined with 3H-thymidine autoradiography. J. Comp. Neurol. 190, 87–114 (1980).
  CAS PubMed Google Scholar
• Skutella, T. & Nitsch, R. New molecules for hippocampal development. Trends Neurosci. 24, 107–113 (2001).
  CAS PubMed Google Scholar
• Gottlieb, D. I. & Cowan, W. M. Evidence for a temporal factor in the occupation of available synaptic sites during the development of the dentate gyrus. Brain Res. 41, 452–456 (1972).
  CAS PubMed Google Scholar
• Bayer, S. A. & Altman, J. Directions in neurogenetic gradients and patterns of anatomical connections in the telencephalon. Prog. Neurobiol. 29, 57–106 (1987).
  CAS Google Scholar
• Zhou, C. F., Li, Y., Morris, R. J. & Raisman, G. Accurate reconstruction of three complementary laminar afferents to the adult hippocampus by embryonic neural grafts. Neurosci. Res. 13 (Suppl.), S43–S53 (1990).
  CAS Google Scholar
• Field, P. M., Seeley, P. J., Frotscher, M. & Raisman, G. Selective innervation of embryonic hippocampal transplants by adult host dentate granule cell axons. Neuroscience 41, 713–727 (1991).
  CAS PubMed Google Scholar
• Li, D., Field, P. M., Strega, U., Li, Y. & Raisman, G. Entorhinal axons project to dentate gyrus in organotypic slice co-culture. Neuroscience 52, 799–813 (1993).
  CAS PubMed Google Scholar
• Li, D., Field, M. & Raisman, G. Connectional specification of regenerating entorhinal projection neuron classes cannot be overridden by altered target availability in postnatal organotypic slice co-culture. Exp. Neurol. 142, 151–160 (1996).
  CAS PubMed Google Scholar
• Frotscher, M. & Heimrich, B. Formation of layer-specific fiber projections to the hippocampus in vitro. Proc. Natl Acad. Sci. USA 90, 10400–10403 (1993).
  CAS PubMed Google Scholar
• Frotscher, M. & Heimrich, B. Lamina-specific synaptic connections of hippocampal neurons in vitro. J. Neurobiol. 26, 350–359 (1995).
  CAS PubMed Google Scholar
• Zhao, S., Förster, E., Chai, X. & Frotscher, M. Different signals control laminar specificity of commissural and entorhinal fibers to the dentate gyrus. J. Neurosci. 23, 7351–7357 (2003). By using co-cultures of wild-type and mutant hippocampus this paper shows that components of the ECM control the lamination of entorhinal fibres to the dentate gyrus. By contrast, positional cues on the target cells guide commissural/associational fibres.
  CAS PubMed Google Scholar
• McConnell, S. K., Ghosh, A. & Shatz, C. J. Subplate neurons pioneer the first axon pathway from the cerebral cortex. Science 245, 978–982 (1989).
  CAS PubMed Google Scholar
• Soriano, E., Del Rio, J. A., Martinez, A. & Super, H. Organization of the embryonic and early postnatal murine hippocampus. I. Immunocytochemical characterization of neuronal populations in the subplate and marginal zone. J. Comp. Neurol. 342, 571–595 (1994).
  CAS PubMed Google Scholar
• Super, H. & Soriano, E. The organization of the embryonic and early postnatal murine hippocampus. II. Development of entorhinal, commissural and septal connections studied with the lipophilic tracer DiI. J. Comp. Neurol. 344, 101–120 (1994).
  CAS PubMed Google Scholar
• Del Rio, J. A. et al. A role for Cajal–Retzius cells and reelin in the development of hippocampal connections. Nature 385, 70–74 (1997). Cajal–Retzius cells are early targets of entorhinal fibres to the hippocampus. Their selective elimination results in misrouting of the entorhino-hippocampal projection.
  CAS PubMed Google Scholar
• Ceranik, K. et al. Hippocampal Cajal–Retzius cells project to the entorhinal cortex: retrograde tracing and intracellular labelling studies. Eur. J. Neurosci. 11, 4278–4290 (1999).
  CAS PubMed Google Scholar
• Super, H., Martinez, A., del Rio, J. A. & Soriano, E. Involvement of distinct pioneer neurons in the formation of layer-specific connections in the hippocampus. J. Neurosci. 18, 4616–4626 (1998).
  CAS PubMed Google Scholar
• Pleasure, S. J. et al. Cell migration from the ganglionic eminences is required for the development of hippocampal GABAergic interneurons. Neuron 26, 727–740 (2000). The laminated termination of entorhinal fibres and commissural/associational fibres to the hippocampus is preserved in the absence of GABAergic interneurons, precluding a role of GABAergic cells as guide posts.
  Google Scholar
• Drakew, A., Frotscher, M. & Heimrich, B. Blockade of neuronal activity alters spine maturation of dentate granule cells but not their dendritic arborization. Neuroscience 94, 767–774 (1999).
  CAS PubMed Google Scholar
• Frotscher, M., Drakew, A. & Heimrich, B. Role of afferent innervation and neuronal activity in dendritic development and spine maturation of fascia dentata granule cells. Cereb. Cortex 10, 946–951 (2000).
  CAS PubMed Google Scholar
• Nitsch, R. & Frotscher, M. Maintenance of peripheral dendrites of GABAergic neurons requires specific input. Brain Res. 554, 304–307 (1991).
  CAS PubMed Google Scholar
• Deller, T. et al. The hippocampus of the reeler mutant mouse: fiber segregation in area CA1 depends on the position of the postsynaptic target cells. Exp. Neurol. 156, 254–267 (1999).
  CAS PubMed Google Scholar
• Deller, T., Drakew, A. & Frotscher, M. Different primary target cells are important for fiber lamination in the fascia dentata: a lesson from reeler mutant mice. Exp. Neurol. 156, 239–253 (1999).
  CAS PubMed Google Scholar
• Stanfield, B. B. & Cowan, W. M. The morphology of the hippocampus and dentate gyrus in normal and reeler mice. J. Comp. Neurol. 185, 393–422 (1979).
  CAS PubMed Google Scholar
• 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). Firmly established a role for VLDLR and APOER2 as receptors for the ECM protein reelin.
  CAS PubMed Google Scholar
• Drakew, A. et al. Dentate granule cells in reeler mutants and VLDLR and ApoER2 knockout mice. Exp. Neurol. 176, 12–24 (2002).
  CAS PubMed Google Scholar
• Gebhardt, C. et al. Abnormal positioning of granule cells alters afferent fiber distribution in the mouse fascia dentata: morphologic evidence from reeler, apolipoprotein E receptor 2-, and very low density lipoprotein receptor knockout mice. J. Comp. Neurol. 445, 278–292 (2002).
  PubMed Google Scholar
• Barbera, A. J., Marchase, R. B. & Roth, S. Adhesive recognition and retinotectal specificity. Proc. Natl Acad. Sci. USA 70, 2482–2486 (1973).
  CAS PubMed Google Scholar
• Gottlieb, D. I., Rock, K. & Glaser, L. A gradient of adhesive specificity in developing avian retina. Proc. Natl Acad. Sci. USA 73, 410–414 (1976).
  CAS PubMed Google Scholar
• Emerling, D. E. & Lander, A. D. Inhibitors and promotors of thalamic neuron adhesion and outgrowth in embryonic neocortex: functional association with chondroitin sulfate. Neuron 17, 1089–1100 (1996).
  CAS PubMed Google Scholar
• Förster, E. et al. Lamina-specific cell adhesion on living slices of hippocampus. Development 125, 3399–3410 (1998).
  PubMed Google Scholar
• Förster, E., Zhao, S. & Frotscher, M. Hyaluronan-associated adhesive cues control fiber segregation in the hippocampus. Development 128, 3029–3039 (2001).
  PubMed Google Scholar
• Grove, E. A., Tole, S., Limon, J., Yip, L. & Ragsdale, C. W. The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in _Gli3_-deficient mice. Development 125, 2315–2325 (1998).
  CAS PubMed Google Scholar
• Rickmann, M., Amaral, D. G. & Cowan, M. Organization of radial glia cells during the development of the rat dentate gyrus. J. Comp. Neurol. 264, 449–479 (1987).
  CAS PubMed Google Scholar
• Altman, J. & Bayer, S. A. Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. J. Comp. Neurol. 301, 325–342 (1990).
  CAS PubMed Google Scholar
• Altman, J. & Bayer, S. A. Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J. Comp. Neurol. 301, 365–381 (1990).
  CAS PubMed Google Scholar
• Pleasure, S. J., Collins, A. E. & Lowenstein, D. H. Unique expression patterns of cell fate molecules delineate sequential stages of dentate gyrus development. J. Neurosci. 20, 6095–6105 (2000).
  CAS PubMed Google Scholar
• Bagri, A. et al. The chemokine SDF1 regulates migration of dentate granule cells. Development 129, 4249–4260 (2002). Characterizes the route of migration of dentate granule cells using in utero retroviral injections. Moreover, the chemokine SDF1 and its receptor CXCR4 were found to regulate granule cell migration.
  CAS PubMed Google Scholar
• Nadarajah, B. & Parnavelas, J. G. Modes of neuronal migration in the developing cerebral cortex. Nature Rev. Neurosci. 3, 423–432 (2002). Describes three modes of neuronal migration: somal translocation in early generated neurons, glia-guided radial migration used by pyramidal cells, and tangential migration of interneurons.
  CAS Google Scholar
• Malatesta, P., Hartfuss, E. & Götz, M. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127, 5253–5263 (2000).
  CAS Google Scholar
• Noctor, S. C., Flint, A. C., Weissman, T. A., Dammerman, R. S. & Kriegstein, A. R. Neurons derived from radial units in neocortex. Nature 409, 714–720 (2001).
  CAS PubMed Google Scholar
• Noctor, S. C. et al. Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J. Neurosci. 22, 3161–3173 (2002).
  CAS PubMed Google Scholar
• Miyata, T., Kawaguchi, A., Okano, H. & Ogawa, M. Assymetric inheritance of radial glial fibers by cortical neurons. Neuron 31, 727–741 (2001).
  CAS PubMed Google Scholar
• Tissir, F. & Goffinet, A. M. Reelin and brain development. Nature Rev. Neurosci. 4, 496–505 (2003). An excellent review of what is known about the function of reelin and the signalling cascades involved.
  CAS Google Scholar
• Zhao, S., Chai, X., Förster, E. & Frotscher, M. Reelin is a positional signal for the lamination of dentate granule cells. Development 131, 5117–5125 (2004). When a slice of reeler hippocampus was co-cultured to a wild-type hippocampal slice the lamination of dentate granule cells was rescued in the reeler slice, showing that reelin needs to be in a specific location to exert its effect on granule cell lamination.
  CAS PubMed Google Scholar
• Howell, B. W., Hawkes, R., Soriano, P. & Cooper, J. A. Neuronal positioning in the developing brain is regulated by mouse disabled-1. Nature 389, 733–737 (1997).
  CAS PubMed Google Scholar
• Förster, 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).
  Google Scholar
• Frotscher, M., Haas, C. & Förster, E. Reelin controls granule cell migration in the dentate gyrus by acting on the radial glial scaffold. Cereb. Cortex 13, 634–640 (2003).
  PubMed Google Scholar
• 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).
  CAS PubMed Google Scholar
• Schwab, M. H. et al. Neuronal basic helix–loop–helix proteins (NEX and BETA2/Neuro D) regulate terminal granule cell differentiation in the hippocampus. J. Neurosci. 20, 3714–3724 (2000).
  CAS PubMed Google Scholar
• Galceran, J., Miyashita-Lin, E. M., Dvaney, E., Rubenstein, J. L. & Grosschedl, R. Hippocampus development and generation of dentate granule cells is regulated by LEF1. Development 127, 469–482 (2000).
  CAS PubMed Google Scholar
• Liu, M. et al. Loss of BETA2/NeuroD leads to malformation of the dentate gyrus and epilepsy. Proc. Natl Acad. Sci. USA 97, 865–870 (2000).
  CAS PubMed Google Scholar
• Del Turco, D. et al. Laminar organization of the mouse dentate gyrus: insights from BETA2/Neuro D mutant mice. J. Comp. Neurol. 477, 81–95 (2004).
  PubMed Google Scholar
• Zhou, C. J., Zhao, C. & Pleasure, S. J. Wnt signaling mutants have decreased dentate granule cell production and radial glial scaffolding abnormalities. J. Neurosci. 24, 121–126 (2004).
  CAS PubMed Google Scholar
• Lee, S. M., Tole, S., Grove, E. & McMahon, A. P. A local Wnt-3a signal is required for development of the mammalian hippocampus. Development 127, 457–467 (2000).
  CAS PubMed Google Scholar
• Pellegrini, M., Mansouri, A., Simeone, A., Boncinelli, E. & Gruss, P. Dentate gyrus formation requires Emx2. Development 122, 3893–3898 (1996).
  CAS PubMed Google Scholar
• Yoshida, M. Emx1 and Emx2 functions in development of dorsal telencephalon. Development 124, 101–111 (1997).
  CAS PubMed Google Scholar
• Porter, F. D. et al. Lhx2, a LIM homeobox gene, is required for eye, forebrain, and definitive erythrocyte development. Development 124, 2935–2944 (1997).
  CAS Google Scholar
• Zhao, Y. et al. Control of hippocampal morphogenesis and neuronal differentiation by the LIM homeobox gene Lhx5. Science 284, 1155–1158 (1999).
  CAS Google Scholar
• Mallamaci, A., Muzio, L., Chan, C. H., Parnavelas, J. & Boncinelli, E. Area identity shifts in the early cerebral cortex of Emx2 −/− mutant mice. Nature Neurosci. 3, 679–686 (2000).
  CAS PubMed Google Scholar
• Tole, S., Goudreau, G., Assimacopoulos, S. & Grove, E. A. Emx2 is required for growth of the hippocampus but not for hippocampal field specification. J. Neurosci. 20, 2618–2625 (2000).
  CAS PubMed Google Scholar
• 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 Google Scholar
• Marin, O., Anderson, S. A. & Rubenstein, J. L. R. Origin and molecular specification of striatal interneurons. J. Neurosci. 20, 6063–6076 (2000).
  CAS PubMed Google Scholar
• Marin-Padilla, M. Cajal–Retzius cells and the development of the neocortex. Trends Neurosci. 21, 64–71 (1998).
  CAS PubMed Google Scholar
• Hevner, R. F., Neogi, T., Englund, C., Daza, R. A. & Fink, A. Cajal–Retzius cells in the mouse: transcription factors, neurotransmitters, and birthdates suggest a pallial origin. Brain Res. Dev. Brain Res. 141, 39–53 (2003).
  CAS PubMed Google Scholar
• Shinozaki, K. et al. Absence of Cajal–Retzius cells and subplate neurons associated with defects of tangential cell migration from ganglionic eminence in Emx1/2 double mutant cerebral cortex. Development 129, 3479–3492 (2002).
  CAS PubMed Google Scholar
• 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 Google Scholar
• Meyer, G. & Wahle, P. The paleocortical ventricle is the origin of reelin-expressing neurons in the marginal zone of the fetal human cortex. Eur. J. Neurosci. 11, 3937–3944 (1999).
  CAS PubMed Google Scholar
• Zecevic, N. & Rakic, P. Development of layer I neurons in the primate cerebral cortex. J. Neurosci. 21, 5607–5619 (2001).
  CAS PubMed Google Scholar
• Meyer, G., Cabrera Socorro, A., Perez Garcia, C. G., Abraham, H. & Caput, D. Expression of p73 and reelin in the developing human cortex. J. Neurosci. 22, 4973–4986 (2002).
  CAS PubMed Google Scholar
• Bielle, F. et al. Multiple origins of Cajal–Retzius cells at the borders of the developing pallium. Nature Neurosci. 8, 1002–1012 (2005).
  CAS PubMed Google Scholar
• Hartmann, D., Sievers, J., Pehlemann, F. W. & Berry, M. Destruction of meningeal cells over the medial cerebral hemisphere of newborn hamsters prevents the formation of the infrapyramidal blade of the dentate gyrus. J. Comp. Neurol. 320, 33–61 (1992).
  CAS PubMed Google Scholar
• Hartmann, D., Frotscher, M. & Sievers, J. Development of granule cells, and afferent and efferent connections of the dentate gyrus after experimentally induced reorganization of the supra- and infrapyramidal blades. Acta Anat. 150, 25–37 (1994).
  CAS PubMed Google Scholar
• Tamamaki, N. Development of afferent fiber lamination in the infrapyramidal blade of the rat dentate gyrus. J. Comp. Neurol. 411, 257–266 (1999).
  CAS PubMed Google Scholar
• Graus-Porta, D. et al. β1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron 31, 367–379 (2001).
  CAS PubMed Google Scholar
• Halfter, W., Dong, S., Yip, Y. P., Willem, M. & Mayer, U. A critical function of the pial basement membrane in cortical histogenesis. J. Neurosci. 22, 6029–6040 (2002).
  CAS PubMed Google Scholar
• Hartmann, D., DeStooper, B. & Saftig, P. Presenilin-1 deficiency leads to loss of Cajal–Retzius neurons and cortical dysplasia similar to human type II lissencephaly. Curr. Biol. 9, 719–727 (1999).
  CAS PubMed Google Scholar
• Niewmierzycka, A., Mills, J., St-Arnaud, R., Dedhar, S. & Reichardt, L. F. Integrin-linked kinase deletion from mouse cortex results in cortical lamination defects resembling cobblestone lissencephaly. J. Neurosci. 25, 7022–7031 (2005).
  CAS PubMed PubMed Central Google Scholar
• Meyer, G. et al. Developmental roles of p73 in Cajal–Retzius cells and cortical patterning. J. Neurosci. 24, 9878–9887 (2004).
  CAS PubMed Google Scholar
• Stumm, R. K. et al. CXCR4 regulates interneuron migration in the developing neocortex. J. Neurosci. 23, 5123–5130 (2003).
  CAS PubMed Google Scholar
• Tissir, F., Wang, C. E. & Goffinet, A. M. Expression of the chemokine receptor CXCR4 mRNA during mouse brain development. Brain Res. Dev. Brain Res. 22, 63–71 (2004).
  Google Scholar
• Verhage, M. et al. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287, 864–869 (2000). Despite the lack of transmitter release in Munc18-1-deficient mice, cortical layers, fibre projections and synaptic structures develop normally.
  CAS Google Scholar
• Ben-Ari, Y. Excitatory actions of GABA during development: the nature of the nurture. Nature Rev. Neurosci. 3, 728–738 (2002).
  CAS Google Scholar
• Houser, C. R. Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. Brain Res. 535, 195–204 (1990).
  CAS PubMed Google Scholar
• Houser, C. R. Neuronal loss and synaptic reorganization in temporal lobe epilepsy. Adv. Neurol. 79, 743–761 (1999).
  CAS PubMed Google Scholar
• 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). The extent of granule cell dispersion in patients with epilepsy was found to correlate with a loss of reelin-synthesizing Cajal–Retzius cells, indicating that reelin could have a role in the maintenance of granule cell lamination in the adult human brain.
  CAS PubMed Google Scholar
• Tauck, D. L. & Nadler, J. V. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J. Neurosci. 5, 1016–1022 (1985).
  CAS PubMed Google Scholar
• Nadler, J. V. The recurrent mossy fiber pathway of the epileptic brain. Neurochem. Res. 28, 1649–1658 (2003).
  CAS PubMed Google Scholar
• 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
• Wenzel, H. J., Robbins, C. A., Tsai, L. H. & Schwartzkroin, P. A. Abnormal morphological and functional organization of the hippocampus in a p35 mutant model of cortical displasia associated with spontaneous seizures. J. Neurosci. 21, 983–998 (2001).
  CAS PubMed Google Scholar
• Walter, J., Kern-Veits, B., Huf, J., Stolze, B. & Bonhoeffer, F. Recognition of position-specific properties of tectal cell membranes by retinal axons in vitro. Development 101, 685–696 (1987).
  CAS PubMed Google Scholar
• Tozuka, Y., Fukuda, S., Namba, T., Seki, T. & Hisatsune, T. GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47, 803–815 (2005).
  CAS PubMed Google Scholar
• Zhao, C., Teng, E. M., Summers, R. G. Jr, Ming, G. -L. & Gage, F. H. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J. Neurosci. 26, 3–11 (2006). The authors used retrovirus-mediated gene transduction to monitor the dendritic and axonal differentiation of adult-born dentate granule cells.
  CAS PubMed Google Scholar
• Blackstad, T. W. Commissural connections of the hippocampal region of the rat, with special reference to their mode of termination. J. Comp. Neurol. 105, 417–537 (1956).
  CAS PubMed Google Scholar
• Blackstad, T. W. On the termination of some afferents to the hippocampus and fascia dentata: an experimental study in the rat. Acta Anat. (Basel) 35, 202–214 (1958).
  CAS Google Scholar
• Deller, T., Martinez, A., Nitsch, R. & Frotscher, M. A novel entorhinal projection to the rat dentate gyrus: direct innervation of proximal dendrites and cell bodies of granule cells and GABAergic interneurons. J. Neurosci. 16, 3322–3333 (1996).
  CAS PubMed Google Scholar
• Ribak, C. E. & Seress, L. Five types of basket cell in the hippocampal dentate gyrus: a combined Golgi and electron microscopic study. J. Neurocytol. 12, 577–597 (1983).
  CAS PubMed Google Scholar
• Soriano, E. & Frotscher, M. A GABAergic axo-axonic cell in the fascia dentata controls the main excitatory hippocampal pathway. Brain Res. 503, 170–174 (1989).
  CAS PubMed Google Scholar
• Han, Z. S., Buhl, E. H., Lorinczi, Z. & Somogyi, P. A high degree of spatial selectivity in the axonal and dendritic domains of physiologically identified local-circuit neurons in the dentate gyrus of the rat hippocampus. Eur. J. Neurosci. 5, 395–410 (1993).
  CAS PubMed Google Scholar
• Soriano, E. & Frotscher, M. GABAergic innervation of the rat fascia dentata: a novel type of interneuron in the granule cell layer with extensive axonal arborization in the molecular layer. J. Comp. Neurol. 334, 385–396 (1993).
  CAS PubMed Google Scholar
• Freund, T. F. & Buzsáki, G. Interneurons of the hippocampus. Hippocampus 6, 347–470 (1996).
  CAS PubMed Google Scholar
• Beffert, U. et al. Reelin and cyclin-dependent kinase 5-dependent signals cooperate in regulating neuronal migration and synaptic transmission. J. Neurosci. 24, 1897–1906 (2004).
  CAS PubMed Google Scholar
• Ohshima, T. et al. Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proc. Natl Acad. Sci. USA 93, 11173–11178 (1996).
  CAS PubMed Google Scholar
• Ko, J. et al. p35 and p39 are essential for cyclin-dependent kinase 5 function during neurodevelopment. J. Neurosci. 395, 510–522 (2001).
  Google Scholar
• Pilz, D. T. et al. LIS1 and XLIS (DCX) mutations cause most classical lissencephaly, but different patterns of malformation. Hum. Mol. Genet. 7, 2029–2037 (1998).
  CAS PubMed Google Scholar
• Francis, F. et al. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 23, 247–256 (1999).
  CAS PubMed Google Scholar
• Corbo, J. C. et al. Doublecortin is required in mice for lamination of the hippocampus but not the neocortex. J. Neurosci. 22, 7548–7557 (2002).
  CAS PubMed Google Scholar
• Bai, J. et al. RNAi reveals doublecortin is required for radial migration in rat neocortex. Nature Neurosci. 6, 1277–1283 (2003).
  CAS PubMed Google Scholar
• Fleck, M. W. et al. Hippocampal abnormalities and enhanced excitability in a murine model of human lissencephaly. J. Neurosci. 20, 2439–2450 (2000).
  CAS PubMed Google Scholar
• Gale, L. M. & McColl, S. R. Chemokines: extracellular messengers for all occasions? Bioessays 21, 17–28 (1999).
  CAS PubMed Google Scholar