Hippocampal development - Old and new findings

Neuroscience

Volumn 248, Issue , 2013, Pages 225-242

  Khalaf Nazzal, R ^a,b   Francis, F ^a,b  

^a INSTITUT DU FER À MOULIN   (France)

^b SORBONNE UNIVERSITÉ   (France)

Author keywords

Connectivity; Medial telencephalon; Migration; Molecular data; Mouse cortical development; Neurogenesis

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; AMPA RECEPTOR; LIM HOMEODOMAIN PROTEIN; TRANSCRIPTION FACTOR LHX2; TRANSCRIPTION FACTOR MSX1; UNCLASSIFIED DRUG; WNT2 PROTEIN; WNT2B PROTEIN; WNT3A PROTEIN; WNT5A PROTEIN;

ANATOMICAL VARIATION; ANTERIOR COMMISSURE; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN MAPPING; CELL COMPARTMENTALIZATION; CELL MIGRATION; ELECTROENCEPHALOGRAM; ELECTROPORATION; ENTORHINAL CORTEX; GLI3 GENE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; HOMEOBOX; HUMAN; IN SITU HYBRIDIZATION; INTERNEURON; INTRACELLULAR SIGNALING; LHX2 GENE; MOLECULAR DYNAMICS; MOSSY FIBER; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM PARAMETERS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; REVIEW; SYNAPTOGENESIS; TELENCEPHALON; ANIMAL; BRAIN DISEASE; CYTOLOGY; DISEASE MODEL; GROWTH, DEVELOPMENT AND AGING; MEMORY; MOUSE; NERVE CELL NETWORK; PATHOLOGY; SPATIAL BEHAVIOR; TRANSGENIC MOUSE;

ANIMALS; BRAIN DISEASES; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; MEMORY; MICE; MICE, TRANSGENIC; NERVE NET; NEURONS; PHENOTYPE; SPATIAL BEHAVIOR;

EID: 84880391038     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.05.061     Document Type: Review

References (140)

1. Alcántara S., Ruiz M., D'Arcangelo G., Ezan F., de Lecea L., Curran T., Sotelo C., Soriano E. Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J Neurosci 1998, 18:7779-7799.
2. Altman J., Bayer S.A. Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. J Comp Neurol 1990, 301:325-342.
3. Altman J., Bayer S.A. Prolonged sojourn of developing pyramidal cells in the intermediate zone of the hippocampus and their settling in the stratum pyramidale. J Comp Neurol 1990, 301:343-364.
4. 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 1990, 301:365-381.
5. Amaral D.G., Dent J.A. Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions. J Comp Neurol 1981, 195:51-86.
6. The hippocampus book 2006, Oxford University Press, USA. P. Andersen, R. Morris, D. Amaral, T. Bliss, J. O'Keefe (Eds.).
7. Angevine J.B. Time of neuron origin in the hippocampal region. An autoradiographic study in the mouse. Exp Neurol 1965, 2(Suppl.):1-70.
8. Angevine J.B., Sidman R.L. Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 1961, 192:766-768.
9. Bagri A., Gurney T., He X., Zou Y.-R., Littman D.R., Tessier-Lavigne M., Pleasure S.J. The chemokine SDF1 regulates migration of dentate granule cells. Development 2002, 129:4249-4260.
10. Bagri A., Cheng H.J., Yaron A., Pleasure S.J., Tessier-Lavigne M. Stereotyped pruning of long hippocampal axon branches triggered by retraction inducers of the semaphorin family. Cell 2003, 113:285-299.
11. Bannerman D.M., Deacon R.M.J., Offen S., Friswell J., Grubb M., Rawlins J.N.P. Double dissociation of function within the hippocampus: spatial memory and hyponeophagia. Behav Neurosci 2002, 116:884-901.
12. Barkovich A.J., Kuzniecky R.I., Jackson G.D., Guerrini R., Dobyns W.B. A developmental and genetic classification for malformations of cortical development. Neurology 2005, 65:1873-1887.
13. Barry G., Piper M., Lindwall C., Moldrich R., Mason S., Little E., Sarkar A., Tole S., Gronostajski R.M., Richards L.J. Specific glial populations regulate hippocampal morphogenesis. J Neurosci 2008, 28:12328-12340.
14. Batista-Brito R., Fishell G. The developmental integration of cortical interneurons into a functional network. Curr Top Dev Biol 2009, 87:81-118.
15. Bayer S.A. Development of the hippocampal region in the rat. I. Neurogenesis examined with 3H-thymidine autoradiography. J Comp Neurol 1980, 190:87-114.
16. Bayer S.A. Development of the hippocampal region in the rat. II. Morphogenesis during embryonic and early postnatal life. J Comp Neurol 1980, 190:115-134.
17. Bazelot M., Simonnet J., Dinocourt C., Bruel-Jungerman E., Miles R., Fricker D., Francis F. Cellular anatomy, physiology and epileptiform activity in the CA3 region of Dcx knockout mice: a neuronal lamination defect and its consequences. Eur J Neurosci 2012, 35:244-256.
18. Ben-Ari Y., Cherubini E., Corradetti R., Gaiarsa J.L. Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol 1989, 416:303-325.
19. Bielle F., Griveau A., Narboux-Nême N., Vigneau S., Sigrist M., Arber S., Wassef M., Pierani A. Multiple origins of Cajal-Retzius cells at the borders of the developing pallium. Nat Neurosci 2005, 8:1002-1012.
20. Borrell V., Río J.A.D., Alcántara S., Derer M., Martínez A., D'Arcangelo G., Nakajima K., Mikoshiba K., Derer P., Curran T., Soriano E. Reelin regulates the development and synaptogenesis of the layer-specific entorhino-hippocampal connections. J Neurosci 1999, 19:1345-1358.
21. Borrell V., Pujadas L., Simó S., Durà D., Solé M., Cooper J.A., Del Río J.A., Soriano E. Reelin and mDab1 regulate the development of hippocampal connections. Mol Cell Neurosci 2007, 36(2):158-173.
22. Bortone D., Polleux F. KCC2 expression promotes the termination of cortical interneuron migration in a voltage-sensitive calcium-dependent manner. Neuron 2009, 62:53-71.
23. Bulchand S., Grove E.A., Porter F.D., Tole S. LIM-homeodomain gene Lhx2 regulates the formation of the cortical hem. Mech Dev 2001, 100:165-175.
24. Butt S.J., Fuccillo M., Nery S., Noctor S., Kriegstein A., Corbin J.G., Fishell G. The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron 2005, 48:591-604.
25. Buzsáki G., Chen L.S., Gage F.H. Spatial organization of physiological activity in the hippocampal region: relevance to memory formation. Prog Brain Res 1990, 83:257-268.
26. Ceranik K., Zhao S., Frotscher M. Development of the entorhino-hippocampal projection: guidance by Cajal-Retzius cell axons. Ann N Y Acad Sci 2000, 911:43-54.
27. Chevaleyre V., Siegelbaum S.A. Strong CA2 pyramidal neuron synapses define a powerful disynaptic cortico-hippocampal loop. Neuron 2010, 66:560-572.
28. Chronister R.B., DeFrance J.F. Organization of projection neurons of the hippocampus. Exp Neurol 1979, 66:509-523.
29. Claiborne B.J., Amaral D.G., Cowan W.M. A light and electron microscopic analysis of the mossy fibers of the rat dentate gyrus. J Comp Neurol 1986, 246:435-458.
30. Corbo J.C., Deuel T.A., Long J.M., LaPorte P., Tsai E., Wynshaw-Boris A., Walsh C.A. Doublecortin is required in mice for lamination of the hippocampus but not the neocortex. J Neurosci 2002, 22:7548-7557.
31. Danglot L., Triller A., Marty S. The development of hippocampal interneurons in rodents. Hippocampus 2006, 16:1032-1060.
32. Datson N.A., Meijer L., Steenbergen P.J., Morsink M.C., Van der Laan S., Meijer O.C., De Kloet E.R. Expression profiling in laser-microdissected hippocampal subregions in rat brain reveals large subregion-specific differences in expression. Eur J Neurosci 2004, 20:2541-2554.
33. Datson N.A., Morsink M.C., Steenbergen P.J., Aubert Y., Schlumbohm C., Fuchs E., De Kloet E.R. A molecular blueprint of gene expression in hippocampal subregions CA1, CA3, and DG is conserved in the brain of the common marmoset. Hippocampus 2009, 19:739-752.
34. Deguchi Y., Donato F., Galimberti I., Cabuy E., Caroni P. Temporally matched subpopulations of selectively interconnected principal neurons in the hippocampus. Nat Neurosci 2011, 14:495-504.
35. Del Río J.A., Martínez A., Fonseca M., Auladell C., Soriano E. Glutamate-like immunoreactivity and fate of Cajal-Retzius cells in the murine cortex as identified with calretinin antibody. Cereb Cortex 1995, 5:13-21.
36. Del Río J.A., Heimrich B., Borrell V., Förster E., Drakew A., Alcántara S., Nakajima K., Miyata T., Ogawa M., Mikoshiba K., Derer P., Frotscher M., Soriano E. A role for Cajal-Retzius cells and reelin in the development of hippocampal connections. Nature 1997, 385:70-74.
37. Des Portes V., Pinard J.M., Billuart P., Vinet M.C., Koulakoff A., Carrié A., Gelot A., Dupuis E., Motte J., Berwald-Netter Y., Catala M., Kahn A., Beldjord C., Chelly J. A novel CNS gene required for neuronal migration and involved in X-linked subcortical laminar heterotopia and lissencephaly syndrome. Cell 1998, 92:51-61.
38. Dong H.-W., Swanson L.W., Chen L., Fanselow M.S., Toga A.W. Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. Proc Natl Acad Sci U S A 2009, 106:11794-11799.
39. Fanselow M.S., Dong H.-W. Are the dorsal and ventral hippocampus functionally distinct structures?. Neuron 2010, 65:7-19.
40. Fleck M.W., Hirotsune S., Gambello M.J., Phillips-Tansey E., Suares G., Mervis R.F., Wynshaw-Boris A., McBain C.J. Hippocampal abnormalities and enhanced excitability in a murine model of human lissencephaly. J Neurosci 2000, 20:2439-2450.
41. Förster E., Zhao S., Frotscher M. Laminating the hippocampus. Nat Rev Neurosci 2006, 7:259-267.
42. Frotscher M., Heimrich B. Formation of layer-specific fiber projections to the hippocampus in vitro. Proc Natl Acad Sci U S A 1993, 90:10400-10403.
43. Frotscher M., Haas C.A., Förster E. Reelin controls granule cell migration in the dentate gyrus by acting on the radial glial scaffold. Cereb Cortex 2003, 13:634-640.
44. Galichet C., Guillemot F., Parras C.M. Neurogenin 2 has an essential role in development of the dentate gyrus. Development 2008, 135:2031-2041.
45. Galimberti I., Bednarek E., Donato F., Caroni P. EphA4 signaling in juveniles establishes topographic specificity of structural plasticity in the hippocampus. Neuron 2010, 65:627-642.
46. Gleeson J.G., Allen K.M., Fox J.W., Lamperti E.D., Berkovic S., Scheffer I., Cooper E.C., Dobyns W.B., Minnerath S.R., Ross M.E., Walsh C.A. Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell 1998, 92:63-72.
47. Gonzales R.B., DeLeon Galvan C.J., Rangel Y.M., Claiborne B.J. Distribution of thorny excrescences on CA3 pyramidal neurons in the rat hippocampus. J Comp Neurol 2001, 430:357-368.
48. Graves A.R., Moore S.J., Bloss E.B., Mensh B.D., Kath W.L., Spruston N. Hippocampal pyramidal neurons comprise two distinct cell types that are countermodulated by metabotropic receptors. Neuron 2012, 76:776-789.
49. Grove E.A., Tole S. Patterning events and specification signals in the developing hippocampus. Cereb Cortex 1999, 9:551-561.
50. 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 1998, 125:2315-2325.
51. Häussler U., Bielefeld L., Froriep U.P., Wolfart J., Haas C.A. Septotemporal position in the hippocampal formation determines epileptic and neurogenic activity in temporal lobe epilepsy. Cereb Cortex 2012, 22:26-36.
52. He X., Treacy M.N., Simmons D.M., Ingraham H.A., Swanson L.W., Rosenfeld M.G. Expression of a large family of POU-domain regulatory genes in mammalian brain development. Nature 1989, 340:35-41.
53. Hébert J.M., Mishina Y., McConnell S.K. BMP signaling is required locally to pattern the dorsal telencephalic midline. Neuron 2002, 35:1029-1041.
54. Hennou S., Khalilov I., Diabira D., Ben-Ari Y., Gozlan H. Early sequential formation of functional GABA(A) and glutamatergic synapses on CA1 interneurons of the rat foetal hippocampus. Eur J Neurosci 2002, 16:197-208.
55. Henze D.A., McMahon D.B.T., Harris K.M., Barrionuevo G. Giant miniature EPSCs at the hippocampal mossy fiber to CA3 pyramidal cell synapse are monoquantal. J Neurophysiol 2002, 87:15-29.
56. Hoch R.V., Rubenstein J.L.R., Pleasure S. Genes and signaling events that establish regional patterning of the mammalian forebrain. Semin Cell Dev Biol 2009, 20:378-386.
57. Hong S.E., Shugart Y.Y., Huang D.T., Shahwan S.A., Grant P.E., Hourihane J.O., Martin N.D., Walsh C.A. Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat Genet 2000, 26:93-96.
58. Hui C.C., Joyner A.L. A mouse model of greig cephalopolysyndactyly syndrome: the extra-toesJ mutation contains an intragenic deletion of the Gli3 gene. Nat Genet 1993, 3:241-246.
59. Imayoshi I., Shimogori T., Ohtsuka T., Kageyama R. Hes genes and neurogenin regulate non-neural versus neural fate specification in the dorsal telencephalic midline. Development 2008, 135:2531-2541.
60. Ishizuka N., Weber J., Amaral D.G. Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J Comp Neurol 1990, 295:580-623.
61. Kappeler C., Saillour Y., Baudoin J.P., Tuy F.P., Alvarez C., Houbron C., Gaspar P., Hamard G., Chelly J., Métin C., Francis F. Branching and nucleokinesis defects in migrating interneurons derived from doublecortin knockout mice. Hum Mol Genet 2006, 15:1387-1400.
62. Kappeler C., Dhenain M., Phan Dinh Tuy F., Saillour Y., Marty S., Fallet-Bianco C., Souville I., Souil E., Pinard J.-M., Meyer G., Encha-Razavi F., Volk A., Beldjord C., Chelly J., Francis F. Magnetic resonance imaging and histological studies of corpus callosal and hippocampal abnormalities linked to doublecortin deficiency. J Comp Neurol 2007, 500:239-254.
63. Keays D.A., Tian G., Poirier K., Huang G.J., Siebold C., Cleak J., Oliver P.L., Fray M., Harvey R.J., Molnár Z., Piñon M.C., Dear N., Valdar W., Brown S.D., Davies K.E., Rawlins J.N., Cowan N.J., Nolan P., Chelly J., Flint J. Mutations in alpha-tubulin cause abnormal neuronal migration in mice and lissencephaly in humans. Cell 2007, 128:45-57.
64. Kjonigsen L.J., Leergaard T.B., Witter M.P., Bjaalie J.G. Digital atlas of anatomical subdivisions and boundaries of the rat hippocampal region. Front Neuroinform 2011, 5:2.
65. Köhler C. Intrinsic connections of the retrohippocampal region in the rat brain. II. The medial entorhinal area. J Comp Neurol 1986, 246:149-169.
66. König N., Valat J., Fulcrand J., Marty R. The time of origin of Cajal-Retzius cells in the rat temporal cortex. An autoradiographic study. Neurosci Lett 1977, 4:21-26.
67. König N., Hornung J.P., Van der Loos H. Identification of Cajal-Retzius cells in immature rodent cerebral cortex: a combined Golgi-EM study. Neurosci Lett 1981, 27:225-229.
68. Lambert de Rouvroit C., Goffinet A.M. The reeler mouse as a model of brain development. Adv Anat Embryol Cell Biol 1998, 150:1-106.
69. Lanore F., Labrousse V.F., Szabo Z., Normand E., Blanchet C., Mulle C. Deficits in morphofunctional maturation of hippocampal mossy fiber synapses in a mouse model of intellectual disability. J Neurosci 2012, 32(49):17882-17893.
70. Laurberg S. Commissural and intrinsic connections of the rat hippocampus. J Comp Neurol 1979, 184:685-708.
71. Lee S.M., Tole S., Grove E., McMahon A.P. A local Wnt-3a signal is required for development of the mammalian hippocampus. Development 2000, 127:457-467.
72. Lein E.S., Zhao X., Gage F.H. Defining a molecular atlas of the hippocampus using DNA microarrays and high-throughput in situ hybridization. J Neurosci 2004, 24:3879-3889.
73. Lein E.S., Hawrylycz M.J., Ao N., Ayres M., Bensinger A., Bernard A., Boe A.F., Boguski M.S., Brockway K.S., Byrnes E.J., et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 2007, 445:168-176.
74. Leinekugel X., Medina I., Khalilov I., Ben-Ari Y., Khazipov R. Ca2+ oscillations mediated by the synergistic excitatory actions of GABA(A) and NMDA receptors in the neonatal hippocampus. Neuron 1997, 18:243-255.
75. Leinekugel X., Khalilov I., Ben-Ari Y., Khazipov R. Giant depolarizing potentials: the septal pole of the hippocampus paces the activity of the developing intact septohippocampal complex in vitro. J Neurosci 1998, 18:6349-6357.
76. Li X.G., Somogyi P., Ylinen A., Buzsáki G. The hippocampal CA3 network: an in vivo intracellular labeling study. J Comp Neurol 1994, 339:181-208.
77. López-Gallardo M., Prada C. Spatial and temporal patterns of morphogenesis of hippocampal pyramidal cells: study in the early postnatal rat. Hippocampus 2001, 11:118-131.
78. Manent J.-B., Demarque M., Jorquera I., Pellegrino C., Ben-Ari Y., Aniksztejn L., Represa A. A noncanonical release of GABA and glutamate modulates neuronal migration. J Neurosci 2005, 25:4755-4765.
79. Manent J.-B., Jorquera I., Ben-Ari Y., Aniksztejn L., Represa A. Glutamate acting on AMPA but not NMDA receptors modulates the migration of hippocampal interneurons. J Neurosci 2006, 26:5901-5909.
80. Mangale V.S., Hirokawa K.E., Satyaki P.R., Gokulchandran N., Chikbire S., Subramanian L., Shetty A.S., Martynoga B., Paul J., Mai M.V., Li Y., Flanagan L.A., Tole S., Monuki E.S. Lhx2 selector activity specifies cortical identity and suppresses hippocampal organizer fate. Science 2008, 319:304-309.
81. Marin O., Anderson S.A., Rubenstein J.L. Origin and molecular specification of striatal interneurons. J Neurosci 2000, 20:6063-6076.
82. Marín O., Valiente M., Ge X., Tsai L.H. Guiding neuronal cell migrations. Cold Spring Harb Perspect Biol 2010, 2:a001834.
83. McManus M.F., Nasrallah I.M., Pancoast M.M., Wynshaw-Boris A., Golden J.A. Lis1 is necessary for normal non-radial migration of inhibitory interneurons. Am J Pathol 2004, 165:775-784.
84. Miles R., Tóth K., Gulyás A.I., Hájos N., Freund T.F. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 1996, 16:815-823.
85. Miyoshi G., Fishell G. GABAergic interneuron lineages selectively sort into specific cortical layers during early postnatal development. Cereb Cortex 2011, 21:845-852.
86. Miyoshi G., Butt S.J.B., Takebayashi H., Fishell G. Physiologically distinct temporal cohorts of cortical interneurons arise from telencephalic Olig2-expressing precursors. J Neurosci 2007, 27:7786-7798.
87. Morozov Y.M., Freund T.F. Postnatal development and migration of cholecystokinin-immunoreactive interneurons in rat hippocampus. Neuroscience 2003, 120:923-939.
88. Muzio L., Soria J.M., Pannese M., Piccolo S., Mallamaci A. A mutually stimulating loop involving emx2 and canonical wnt signalling specifically promotes expansion of occipital cortex and hippocampus. Cereb Cortex 2005, 15:2021-2028.
89. Nadarajah B., Brunstrom J.E., Grutzendler J., Wong R.O.L., Pearlman A.L. Two modes of radial migration in early development of the cerebral cortex. Nat Neurosci 2001, 4:143-150.
90. Nakahira E., Yuasa S. Neuronal generation, migration, and differentiation in the mouse hippocampal primoridium as revealed by enhanced green fluorescent protein gene transfer by means of in utero electroporation. J Comp Neurol 2005, 483:329-340.
91. Navarro-Quiroga I., Chittajallu R., Gallo V., Haydar T.F. Long-term, selective gene expression in developing and adult hippocampal pyramidal neurons using focal in utero electroporation. J Neurosci 2007, 27:5007-5011.
92. Nery S., Fishell G., Corbin J.G. The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat Neurosci 2002, 5:1279-1287.
93. Newrzella D., Pahlavan P.S., Krüger C., Boehm C., Sorgenfrei O., Schröck H., Eisenhardt G., Bischoff N., Vogt G., Wafzig O., Rossner M., Maurer M.H., Hiemisch H., Bach A., Kuschinsky W., Schneider A. The functional genome of CA1 and CA3 neurons under native conditions and in response to ischemia. BMC Genomics 2007, 8:370.
94. Nosten-Bertrand M., Kappeler C., Dinocourt C., Denis C., Germain J., Phan Dinh Tuy F., Verstraeten S., Alvarez C., Métin C., Chelly J., Giros B., Miles R., Depaulis A., Francis F. Epilepsy in Dcx knockout mice associated with discrete lamination defects and enhanced excitability in the hippocampus. PLoS One 2008, 3:e2473.
95. Nowakowski R.S., Rakic P. The mode of migration of neurons to the hippocampus: a Golgi and electron microscopic analysis in foetal rhesus monkey. J Neurocytol 1979, 8:697-718.
96. O'Leary D.D., Bicknese A.R., De Carlos J.A., Heffner C.D., Koester S.E., Kutka L.J., Terashima T. Target selection by cortical axons: alternative mechanisms to establish axonal connections in the developing brain. Cold Spring Harb Symp Quant Biol 1990, 55:453-468.
97. Petrovich G.D., Canteras N.S., Swanson L.W. Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems. Brain Res Brain Res Rev 2001, 38:247-289.
98. Picardo M.A., Guigue P., Bonifazi P., Batista-Brito R., Allene C., Ribas A., Fishell G., Baude A., Cossart R. Pioneer GABA cells comprise a subpopulation of hub neurons in the developing hippocampus. Neuron 2011, 71:695-709.
99. Pierani A., Wassef M. Cerebral cortex development: from progenitors patterning to neocortical size during evolution. Dev Growth Differ 2009, 51:325-342.
100. Pleasure S.J., Anderson S., Hevner R., Bagri A., Marin O., Lowenstein D.H., Rubenstein J.L. Cell migration from the ganglionic eminences is required for the development of hippocampal GABAergic interneurons. Neuron 2000, 28:727-740.
101. Polleux F., Whitford K.L., Dijkhuizen P.A., Vitalis T., Ghosh A. Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling. Development 2002, 129:3147-3160.
102. Ramírez-Amaya V., Balderas I., Sandoval J., Escobar M.L., Bermúdez-Rattoni F. Spatial long-term memory is related to mossy fiber synaptogenesis. J Neurosci 2001, 21:7340-7348.
103. Reiner O., Carrozzo R., Shen Y., Wehnert M., Faustinella F., Dobyns W.B., Caskey C.T., Ledbetter D.H. Isolation of a Miller-Dieker lissencephaly gene containing G protein beta-subunit-like repeats. Nature 1993, 364:717-721.
104. Rivera C., Voipio J., Payne J.A., Ruusuvuori E., Lahtinen H., Lamsa K., Pirvola U., Saarma M., Kaila K. The K+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 1999, 397:251-255.
105. Rollenhagen A., Sätzler K., Rodríguez E.P., Jonas P., Frotscher M., Lübke J.H.R. Structural determinants of transmission at large hippocampal mossy fiber synapses. J Neurosci 2007, 27:10434-10444.
106. Rubin A.N., Alfonsi F., Humphreys M.P., Choi C.K.P., Rocha S.F., Kessaris N. The germinal zones of the basal ganglia but not the septum generate GABAergic interneurons for the cortex. J Neurosci 2010, 30:12050-12062.
107. Schimmang T., Lemaistre M., Vortkamp A., Rüther U. Expression of the zinc finger gene Gli3 is affected in the morphogenetic mouse mutant extra-toes (Xt). Development 1992, 116:799-804.
108. Sekino Y., Obata K., Tanifuji M., Mizuno M., Murayama J. Delayed signal propagation via CA2 in rat hippocampal slices revealed by optical recording. J Neurophysiol 1997, 78:1662-1668.
109. Sheldon M., Rice D.S., D'Arcangelo G., Yoneshima H., Nakajima K., Mikoshiba K., Howell B.W., Cooper J.A., Goldowitz D., Curran T. Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature 1997, 389:730-733.
110. Shimogori T., Banuchi V., Ng H.Y., Strauss J.B., Grove E.A. Embryonic signaling centers expressing BMP, WNT and FGF proteins interact to pattern the cerebral cortex. Development 2004, 131:5639-5647.
111. Slomianka L., Amrein I., Knuesel I., Sørensen J.C., Wolfer D.P. Hippocampal pyramidal cells: the reemergence of cortical lamination. Brain Struct Funct 2011, 216:301-317.
112. Sommer L., Ma Q., Anderson D.J. Neurogenins, a novel family of atonal-related bHLH transcription factors, are putative mammalian neuronal determination genes that reveal progenitor cell heterogeneity in the developing CNS and PNS. Mol Cell Neurosci 1996, 8:221-241.
113. Soriano E., Cobas A., Fairén A. Asynchronism in the neurogenesis of GABAergic and non-GABAergic neurons in the mouse hippocampus. Brain Res 1986, 395:88-92.
114. Soriano E., Cobas A., Fairén A. Neurogenesis of glutamic acid decarboxylase immunoreactive cells in the hippocampus of the mouse. I: regio superior and regio inferior. J Comp Neurol 1989, 281:586-602.
115. Soriano E., Cobas A., Fairén A. Neurogenesis of glutamic acid decarboxylase immunoreactive cells in the hippocampus of the mouse. II: area dentata. J Comp Neurol 1989, 281:603-611.
116. Spruston N. Pyramidal neurons: dendritic structure and synaptic integration. Nat Rev Neurosci 2008, 9:206-221.
117. Stanfield B.B., Cowan W.M. The development of the hippocampus and dentate gyrus in normal and reeler mice. J Comp Neurol 1979, 185:423-459.
118. Steward O. Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat. J Comp Neurol 1976, 167:285-314.
119. Subramanian L., Tole S. Mechanisms underlying the specification, positional regulation, and function of the cortical hem. Cereb Cortex 2009, 19(Suppl. 1):i90-i95.
120. Subramanian L., Remedios R., Shetty A., Tole S. Signals from the edges: the cortical hem and antihem in telencephalic development. Semin Cell Dev Biol 2009, 20(6):712-718.
121. Supèr H., Martínez A., Del Río J.A., Soriano E. Involvement of distinct pioneer neurons in the formation of layer-specific connections in the hippocampus. J Neurosci 1998, 18:4616-4626.
122. Tabata H., Nakajima K. Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J Neurosci 2003, 23:9996-10001.
123. Thompson C.L., Pathak S.D., Jeromin A., Ng L.L., MacPherson C.R., Mortrud M.T., Cusick A., Riley Z.L., Sunkin S.M., Bernard A., Puchalski R.B., Gage F.H., Jones A.R., Bajic V.B., Hawrylycz M.J., Lein E.S. Genomic anatomy of the hippocampus. Neuron 2008, 60:1010-1021.
124. Tole S., Grove E.A. Detailed field pattern is intrinsic to the embryonic mouse hippocampus early in neurogenesis. J Neurosci 2001, 21:1580-1589.
125. Tole S., Christian C., Grove E.A. Early specification and autonomous development of cortical fields in the mouse hippocampus. Development 1997, 124:4959-4970.
126. Tricoire L., Pelkey K.A., Erkkila B.E., Jeffries B.W., Yuan X., McBain C.J. A blueprint for the spatiotemporal origins of mouse hippocampal interneuron diversity. J Neurosci 2011, 3:10948-10970.
127. Trommsdorff M., Gotthardt M., Hiesberger T., Shelton J., Stockinger W., Nimpf J., Hammer R.E., Richardson J.A., Herz J. Reeler/disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 1999, 97:689-701.
128. Tyzio R., Represa A., Jorquera I., Ben-Ari Y., Gozlan H., Aniksztejn L. The establishment of GABAergic and glutamatergic synapses on CA1 pyramidal neurons is sequential and correlates with the development of the apical dendrite. J Neurosci 1999, 19:10372-10382.
129. Van Groen T., Miettinen P., Kadish I. The entorhinal cortex of the mouse: organization of the projection to the hippocampal formation. Hippocampus 2003, 13:133-149.
130. Van Praag H., Kempermann G., Gage F.H. Neural consequences of environmental enrichment. Nat Rev Neurosci 2000, 1:191-198.
131. Van Strien N.M., Cappeart N., Witter M.P. The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network. Nat Rev Neurosci 2009, 10:272-282.
132. Verney C., Takahashi T., Bhide P.G., Nowakowski R.S., Caviness V.S. Independent controls for neocortical neuron production and histogenetic cell death. Dev Neurosci 2000, 22:125-138.
133. 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 2001, 128:3759-3771.
134. Williams M.E., Wilke S.A., Daggett A., Davis E., Otto S., Ravi D., Ripley B., Bushong E.A., Ellisman M.H., Klein G., Ghosh A. Cadherin-9 regulates synapse-specific differentiation in the developing hippocampus. Neuron 2011, 71:640-655.
135. Wyszynski M., Lin J., Rao A., Nigh E., Beggs A.H., Craig A.M., Sheng M. Competitive binding of alpha-actinin and calmodulin to the NMDA receptor. Nature 1997, 385:439-442.
136. Xu N.J., Henkemeyer M. Ephrin-B3 reverse signaling through Grb4 and cytoskeletal regulators mediates axon pruning. Nat Neurosci 2009, 12:268-276.
137. Yabut O., Renfro A., Niu S., Swann J.W., Marin O., D'Arcangelo G. Abnormal laminar position and dendrite development of interneurons in the reeler forebrain. Brain Res 2007, 1140:75-83.
138. Yoshida M., Assimacopoulos S., Jones K.R., Grove E.A. Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order. Development 2006, 133:537-545.
139. Zhao S., Förster E., Chai X., Frotscher M. Different signals control laminar specificity of commissural and entorhinal fibers to the dentate gyrus. J Neurosci 2003, 23(19):7351-7357.
140. Zhao S., Chai X., Förster E., Frotscher M. Reelin is a positional signal for the lamination of dentate granule cells. Development 2004, 131(20):5117-5125.