Control of cortical neuronal migration by glutamate and GABA

Frontiers in Cellular Neuroscience

Volumn 9, Issue JAN, 2015, Pages

  Luhmann, Heiko J ^a   Fukuda, A ^b   Kilb, W ^a  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Cerebral cortex; GABA; Glutamate; Neuronal migration; Neuronal migration disorders

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA2; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA3; 4 AMINOBUTYRIC ACID RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALRETININ; CHEMOKINE RECEPTOR CXCR4; CHOLECYSTOKININ; CONNEXIN 26; CONNEXIN 43; DEXTRO SERINE; DOUBLECORTIN; EPHRIN RECEPTOR A4; EPHRIN RECEPTOR A5; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLUTAMIC ACID; GLYCINE; GLYCINE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROPEPTIDE Y; REELIN; STROMAL CELL DERIVED FACTOR 1; TAURINE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DLX1; TRANSCRIPTION FACTOR DLX2; TRANSCRIPTION FACTOR MASH1; UNCLASSIFIED DRUG; UNINDEXED DRUG; VASOACTIVE INTESTINAL POLYPEPTIDE;

BRAIN CELL; BRAIN DEVELOPMENT; CELL MIGRATION; CYTOSKELETON; EXTRACELLULAR SPACE; GENETIC MANIPULATION; HUMAN; INTERNEURON; MACROGLIA; MENTAL DISEASE; NEUROLOGIC DISEASE; NEURONAL MIGRATION DISORDER; NONHUMAN; PYRAMIDAL NERVE CELL; REVIEW;

EID: 84922141441     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2015.00004     Document Type: Review

References (136)

1. Allene, C., and Cossart, R. (2010). Early NMDA receptor-driven waves of activity in the developing neocortex: physiological or pathological network oscillations? J. Physiol. 588, 83-91. doi: 10.1113/jphysiol.2009.178798
2. Avila, A., Vidal, P. M., Dear, T. N., Harvey, R. J., Rigo, J. M., and Nguyen, L. (2013). Glycine receptor alpha 2 subunit activation promotes cortical interneuron migration. CellRep. 4, 738-750. doi: 10.1016/j.celrep.2013.07.016
3. Ayala, R., Shu, T., and Tsai, L. H. (2007). Trekking across the brain: the journey of neuronal migration. Cell 128, 29-43. doi: 10.1016/j.cell.2006.12.021
4. Bagnard, D., Vaillant, C., Khuth, S. T., Dufay, N., Lohrum, M., Puschel, A. W., et al. (2001). Semaphorin 3A-vascular endothelial growth factor-165 balance mediates migration and apoptosis of neural progenitor cells by the recruitment of shared receptor. J. Neurosci. 21, 3332-3341.
5. Bahn, S., Volk, B., and Wisden, W. (1994). Kainate receptor gene expression in the developing rat brain. J. Neurosci. 14, 5525-5547.
6. Behar, T. N., Li, Y. X., Tran, H. T., Ma, W., Dunlap, V., Scott, C., et al. (1996). GABA stimulates chemotaxis and chemokinesis of embryonic cortical neurons via calcium-dependent mechanisms. J. Neurosci. 16, 1808-1818.
7. Behar, T. N., Schaffner, A. E., Scott, C. A., Greene, C. L., and Barker, J. L. (2000).GABAreceptorantagonists modulate postmitotic cell migration in slice cultures of embryonic rat cortex. Cereb. Cortex 10, 899-909. doi: 10.1093/cercor/10.9.899
8. Behar, T. N., Schaffner, A. E., Scott, C. A., O'Connell, C., and Barker, J. L. (1998). Differential response of cortical plate and ventricular zone cells to GABA as a migration stimulus. J. Neurosci. 18, 6378-6387.
9. Behar, T. N., Smith, S. V., Kennedy, R. T., Mckenzie, J. M., Maric, I., and Barker, A. L. (2001). GABAB receptors mediate motilitysignals formigrating embryonic cortical cells. Cereb. Cortex 11, 744-753. doi: 10.1093/cercor/11.8.744
10. Ben-Ari, Y., Gaiarsa, J. L., Tyzio, R., and Khazipov, R. (2007). GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol. Rev. 87, 1215-1284. doi: 10.1152/physrev.00017.2006
11. Bolteus, A. J., Garganta, C., and Bordey, A. (2005). Assays for measuring extracellular GABAlevels and cell migration rate in acute slices. Brain Res. Brain Res. Protoc. 14, 126-134. doi: 10.1016/j.brainresprot.2004.12.005
12. Bony, G., Szczurkowska, J., Tamagno, I., Shelly, M., Contestabile, A., and Cancedda, L. (2013). Non-hyperpolarizing GABA(B) receptor activation regulates neuronal migration and neurite growth and specification by cAMP/LKB1. Nat. Commun. 4:1800. doi: 10.1038/ncomms2820
13. Borrell, V., and Marin, O. (2006). Meninges control tangential migration of hem-derived Cajal-Retzius cells via CXCL12/CXCR4 signaling. Nat. Neurosci. 9, 1284-1293. doi: 10.1038/nn1764
14. Bortone, D., and Polleux, F. (2009). KCC2 expression promotes the termination of cortical interneuron migration in a voltage-sensitive calcium-dependent manner. Neuron 62, 53-71. doi: 10.1016/j.neuron.2009.01.034
15. Butt, S. J. B., Cobos, I., Golden, J., Kessaris, N., Pachnis, V., and Anderson, S. (2007). Transcriptional regulation of cortical interneuron development. J.Neurosci. 27, 11847-11850. doi: 10.1523/jneurosci.3525-07.2007
16. Butt, S. J., Fuccillo, M., Nery, S., Noctor, S., Kriegstein, A., Corbin, J. G., et al. (2005). The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron 48, 591-604. doi: 10.1016/j.neuron.2005.09.034
17. Bystron, I., Blakemore, C., and Rakic, P. (2008). Development of the human cerebral cortex: Boulder committee revisited. Nat. Rev. Neurosci. 9, 110-122. doi: 10.1038/nrn2252
18. Cancedda, L., Fiumelli, H., Chen, K., and Poo, M. M. (2007). Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo. J. Neurosci. 27, 5224-5235. doi: 10.1523/jneurosci.5169-06.2007
19. Carlson, V. C. C., and Yeh, H. H. (2011). GABA(A) receptor subunit profiles of tangentially migrating neurons derived from the medial ganglionic eminence. Cereb. Cortex 21, 1792-1802. doi: 10.1093/cercor/bhq247
20. Chandrasekar, R. (2013). Alcohol and NMDAreceptor: current research and future direction. Front. Mol. Neurosci. 6:14. doi: 10.3389/fnmol.2013.00014
21. Cina, C., Maass, K., Theis, M., Willecke, K., Bechberger, J. F., and Naus, C. C. (2009). Involvement of the cytoplasmic C-terminal domain of connexin43 in neuronal migration. J. Neurosci. 29, 2009-2021. doi: 10.1523/jneurosci.5025-08.2009
22. Cooper, J. A. (2008). A mechanism for inside-out lamination in the neocortex. Trends Neurosci. 31, 113-119. doi: 10.1016/j.tins.2007.12.003
23. Crandall, J. E., McCarthy, D. M., Araki, K. Y., Sims, J. R., Ren, J.-Q., and Bhide, P. G. (2007). Dopamine receptoractivation modulates GABAneuron migration from the basal forebrain to the cerebral cortex. J. Neurosci. 27, 3813-3822. doi: 10.1523/jneurosci.5124-06.2007
24. Cuzon, V. C., Yeh, P. W., Cheng, Q., and Yeh, H. H. (2006). Ambient GABA promotes cortical entry of tangentially migrating cells derived from the medial ganglionic eminence. Cereb. Cortex 16, 1377-1388. doi: 10.1093/cercor/bhj084
25. Cuzon, V. C., Yeh, P. W., Yanagawa, Y., Obata, K., and Yeh, H. H. (2008). Ethanol consumption during early pregnancy alters the disposition of tangentially migrating GABAergic interneurons in the fetal cortex. J. Neurosci. 28, 1854-1864. doi: 10.1523/jneurosci.5110-07.2008
26. de Carlos, J. A., Lopez-Mascaraque, L., and Valverde, F. (1996). Dynamics of cell migration from the lateral ganglionic eminence in the rat. J. Neurosci. 16, 6146-6156.
27. de Lima, A. D., Gieseler, A., and Voigt, T. (2009). Relationship between GABAergic interneurons migration and early neocortical network activity. Dev. Neurobiol. 69, 105-123. doi: 10.1002/dneu.20696
28. Denter, D. G., Heck, N., Riedemann, T., White, R., Kilb, W., and Luhmann, H. J. (2010). GABA(C) receptors are functionally expressed in the intermediate zone and regulate radial migration in the embryonic mouse neocortex. Neuroscience 167, 124-134. doi: 10.1016/j.neuroscience.2010.01.049
29. Dvorzhak, A., Myakhar, O., Unichenko, P., Kirmse, K., and Kirischuk, S. (2010). Estimation of ambient GABA levels in layer I of the mouse neonatal cortex in brain slices. J. Physiol. 588, 2351-2360. doi: 10.1113/jphysiol.2010.187054
30. Elias, L. A., and Kriegstein, A. R. (2008). Gap junctions: multifaceted regulators of embryonic cortical development. Trends Neurosci. 31, 243-250. doi: 10.1016/j.tins.2008.02.007
31. Elias, L. A., Turmaine, M., Parnavelas, J. G., and Kriegstein, A. R. (2010). Connexin 43 mediates the tangential to radial migratoryswitch in ventrallyderived cortical interneurons. J. Neurosci. 30, 7072-7077. doi: 10.1523/jneurosci.5728-09.2010
32. Elias, L. A., Wang, D. D., and Kriegstein, A. R. (2007). Gap junction adhesion is necessary for radial migration in the neocortex. Nature 448, 901-907. doi: 10.1038/nature06063
33. Fahrion, J. K., Komuro, Y., Li, Y., Ohno, N., Littner, Y., Raoult, E., et al. (2012). Rescue of neuronal migration deficits in a mouse model of fetal Minamata disease by increasing neuronal Ca2+ spike frequency. Proc. Natl. Acad. Sci. USA 109, 5057-5062. doi: 10.1073/pnas.1120747109
34. Farrant, M., and Kaila, K. (2007). The cellular, molecular and ionic basis of GABA(A) receptor signalling. Prog. Brain Res. 160, 59-87. doi: 10.1016/s0079-6123(06)60005-8
35. Flint, A. C., Liu, X. L., and Kriegstein, A. R. (1998). Nonsynaptic glycine receptor activation during early neocortical development. Neuron 20, 43-53. doi: 10.1016/s0896-6273(00)80433-x
36. Friocourt, G., Liu, J. S., Antypa, M., Rakic, S., Walsh, C. A., and Parnavelas, J. G. (2007). Both doublecortin and doublecortin-like kinase play a role in cortical interneuron migration. J. Neurosci. 27, 3875-3883. doi: 10.1523/jneurosci.4530-06.2007
37. Furukawa, T., Yamada, J., Akita, T., Matsushima, Y., Yanagawa, Y., and Fukuda, A. (2014). Roles oftaurine-mediated tonic GABAAreceptoractivation in the radial migration of neurons in the fetal mouse cerebral cortex. Front. Cell. Neurosci. 8:88. doi: 10.3389/fncel.2014.00088
38. Gelman, D. M., and Marin, O. (2010). Generation of interneuron diversity in the mouse cerebral cortex. Eur. J. Neurosci. 31, 2136-2141. doi: 10.1111/j.1460-9568.2010.07267.x
39. Gerber, A. M., Beaman-Hall, C. M., Mathur, A., and Vallano, M. L. (2010). Reduced blockade by extracellular Mg2+ is permissive to NMDA receptor activation in cerebellar granule neurons that model a migratory phenotype. J. Neurochem. 114, 191-202. doi: 10.1111/j.1471-4159.2010.06746.x
40. Gleeson, J. G., and Walsh, C. A. (2000). Neuronal migration disorders: from genetic diseases to developmental mechanisms. Trends Neurosci. 23, 352-359. doi: 10.1016/s0166-2236(00)01607-6
41. Gressens, P., Baes, M., Leroux, P., Lombet, A., Van Veldhoven, P., Janssen, A., et al. (2000). Neuronal migration disorder in Zellweger mice is secondary to glutamate receptor dysfunction. Ann. Neurol. 48, 336-343. doi: 10.1002/1531-8249(200009)48:3<336::aid-ana8>3.0.co;2-q
42. Guerrini, R., Dobyns, W. B., and Barkovich, A. J. (2008). Abnormal development of the human cerebral cortex: genetics, functional consequences and treatment options. Trends Neurosci. 31, 154-162. doi: 10.1016/j.tins.2007.12.004
43. Guerrini, R., and Parrini, E. (2010). Neuronal migration disorders. Neurobiol. Dis.38, 154-166. doi: 10.1016/j.nbd.2009.02.008
44. Heck, N., Kilb, W., Reiprich, P., Kubota, H., Furukawa, T., Fukuda, A., et al. (2007).GABA-A receptors regulate neocortical neuronal migration in vitro and in vivo. Cereb. Cortex 17, 138-148. doi: 10.1093/cercor/bhj135
45. Hirai, K., Yoshioka, H., Kihara, M., Hasegawa, K., Sakamoto, T., Sawada, T., et al. (1999). Inhibiting neuronal migration by blocking NMDA receptors in the embryonic rat cerebral cortex: a tissue culture study. Brain Res. Dev. Brain Res. 114, 63-67. doi: 10.1016/s0165-3806(99)00019-x
46. Holmberg, J., Genander, M., Halford, M. M., Anneren, C., Sondell, M., Chumley, M. J., et al. (2006). EphB receptors coordinate migration and proliferation in the intestinal stem cell niche. Cell 125, 1151-1163. doi: 10.1016/j.cell.2006.04.030
47. Huang, Z. (2009). Molecular regulation of neuronal migration during neocortical development. Mol. Cell. Neurosci. 42, 11-22. doi: 10.1016/j.mcn.2009.06.003
48. Ikonomidou, C., and Turski, L. (2010). Antiepileptic drugs and brain development. EpilepsyRes. 88, 11-22. doi: 10.1016/j.eplepsyres.2009.09.019
49. Inada, H., Watanabe, M., Uchida, T., Ishibashi, H., Wake, H., Nemoto, T., et al.. GABA regulates the multidirectional tangential migration ofGABAergic interneurons in living neonatal mice. Plos One 6:e27048. doi: 10.1371/journal.pone.0027048
50. Inoue, K., Furukawa, T., Kumada, T., Yamada, J., Wang, T. Y., Inoue, R., et al.. Taurine inhibits K+-Cl-cotransporter KCC2 to regulate embryonic Cl-homeostasis via With-no-lysine (WNK) protein kinase signaling pathway. J. Biol. Chem. 287, 20839-20850. doi: 10.1074/jbc.m111.319418
51. Inta, D., Alfonso, J., von Engelhardt, J., Kreuzberg, M. M., Meyer, A. H., van Hooft, J. A., et al. (2008). Neurogenesis and widespread forebrain migration ofdistinct GABAergic neurons from the postnatal subventricular zone. Proc. Natl. Acad. Sci. U S A 105, 20994-20999. doi: 10.1073/pnas.0807059105
52. Iwasato, T., Datwani, A., Wolf, A. M., Nishiyama, H., Taguchi, Y., Tonegawa, S., et al. (2000). Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex. Nature 406, 726-731. doi: 10.1038/35021059
53. Jansson, L. C., Louhivuori, L., Wigren, H. K., Nordstrom, T., Louhivuori, V., Castren, M. L., et al. (2013). Effect of glutamate receptor antagonists on migrating neural progenitor cells. Eur. J. Neurosci. 37, 1369-1382. doi: 10.1111/ejn.12152
54. Ji, F. Y., Kanbara, N., and Obata, K. (1999). GABA and histogenesis in fetal and neonatal mouse brain lacking both the isoforms ofglutamic acid decarboxylase. Neurosci. Res. 33, 187-194. doi: 10.1016/s0168-0102(99)00011-5
55. Jovanovic, J. N., and Thomson, A. M. (2011). Development of cortical GABAergic innervation. Front. Cell. Neurosci. 5:14. doi: 10.3389/fncel.2011.00014
56. Kaila, K. (2014). Cation-chloride cotransporters in neuronal development, plasticityand disease. Nat. Rev. Neurosci. 15, 637-654. doi: 10.1038/nrn3819
57. Khazipov, R., and Luhmann, H. J. (2006). Earlypatterns ofelectrical activityin the developing cerebral cortexofhuman and rodents. Trends Neurosci. 29, 414-418. doi: 10.1016/j.tins.2006.05.007
58. Kholmanskikh, S. S., Koeller, H. B., Wynshaw-Boris, A., Gomez, T., Letourneau, P. C., and Ross, M. E. (2006). Calcium-dependent interaction of lis1 with IQGAP1 and Cdc42 promotes neuronal motility. Nat. Neurosci. 9, 50-57.doi: 10.1038/nn1619
59. Kihara, M., Yoshioka, H., Hirai, K., Hasegawa, K., Kizaki, Z., and Sawada, T. (2002). Stimulation of N-methyl-D-aspartate (NMDA) receptors inhibits neuronal migration in embryonic cerebral cortex: a tissue culture study. Brain Res. Dev. Brain Res. 138, 195-198. doi: 10.1016/s0165-3806(02)00490-x
60. Kilb, W. (2012). Development of the GABAergic system from birth to adolescence. Neuroscientist 18, 613-630. doi: 10.1177/1073858411422114
61. Kilb, W., Hanganu, I. L., Okabe, A., Sava, B. A., Shimizu-Okabe, C., Fukuda, A., et al. (2008). Glycine receptors mediate excitation of subplate neurons in neonatal rat cerebral cortex. J. Neurophysiol. 100, 698-707. doi: 10.1152/jn.00657.2007
62. Kilb, W., Ikeda, M., Uchida, K., Okabe, A., Fukuda, A., and Luhmann, H. J. (2002). Depolarizing glycine responses in Cajal-Retzius cells of neonatal rat cerebral cortex. Neuroscience 112, 299-307. doi: 10.1016/s0306-4522(02)00071-4
63. Kilb, W., Kirischuk, S., and Luhmann, H. J. (2011). Electrical activity patterns and the functional maturation of the neocortex. Eur. J. Neurosci. 34, 1677-1686. doi: 10.1111/j.1460-9568.2011.07878.x
64. Kilb, W., Kirischuk, S., and Luhmann, H. J. (2013). Role of tonic GABAergic currents during pre-and early postnatal rodent development. Front. Neural Circuits 7:139. doi: 10.3389/fncir.2013.00139
65. Kim, P. M., Aizawa, H., Kim, P. S., Huang, A. S., Wickramasinghe, S. R., Kashani, A. H., et al. (2005). Serine racemase: activation byglutamate neurotransmission viaglutamate receptor interactingprotein and mediation ofneuronal migration. Proc. Natl. Acad. Sci. U S A 102, 2105-2110. doi: 10.1073/pnas.0409723102
66. Kirischuk, S., and Kilb, W. (2012). "GAT (GABA transporters)," in Encyclopedia of Signaling Molecules, ed C. Sangdun (New York: Springer), 756-760.
67. Kirischuk, S., Luhmann, H. J., and Kilb, W. (2014). Cajal-Retzius cells: update on structural and functional properties of these mystic neurons that bridged the 20th century. Neuroscience 275, 33-46. doi: 10.1016/j.neuroscience.2014.06.009
68. Koizumi, H., Tanaka, T., and Gleeson, J. G. (2006). Doublecortin-like kinase functions with doublecortin to mediate fiber tract decussation and neuronal migration. Neuron 49, 55-66. doi: 10.1016/j.neuron.2005.10.040
69. Kojima, T., Hirota, Y., Ema, M., Takahashi, S., Miyoshi, I., Okano, H., et al. (2010). Subventricular zone-derived neural progenitor cells migrate along a blood vessel scaffold toward the post-stroke striatum. Stem Cells 28, 545-554. doi: 10.1002/stem.306
70. Komuro, H., and Kumada, T. (2005). Ca2+ transients control CNS neuronal migration. Cell Calcium 37, 387-393. doi: 10.1016/j.ceca.2005.01.006
71. Komuro, H., and Rakic, P. (1993). Modulation of neuronal migration by NMDA receptors. Science 260, 95-97. doi: 10.1126/science.8096653
72. Komuro, H., and Rakic, P. (1996). Intracellular Ca2+ fluctuations modulate the rate of neuronal migration. Neuron 17, 275-285. doi: 10.1016/s0896-6273(00)80159-2
73. Koyama, R., Tao, K., Sasaki, T., Ichikawa, J., Miyamoto, D., Muramatsu, R., et al. (2012). GABAergic excitation after febrile seizures induces ectopic granule cells and adult epilepsy. Nat. Med. 18, 1271-1278. doi: 10.1038/nm.2850
74. Kumada, T., and Komuro, H. (2004). Completion ofneuronal migration regulated by loss of Ca(2+) transients. Proc. Natl. Acad. Sci. USA 101, 8479-8484. doi: 10.1073/pnas.0401000101
75. Kumada, T., Lakshmana, M. K., and Komuro, H. (2006). Reversal of neuronal migration in a mouse model of fetal alcohol syndrome by controlling second-messenger signalings. J. Neurosci. 26, 742-756. doi: 10.1523/jneurosci.4478-05.2006
76. Kwan, K. Y., Sestan, N., and Anton, E. S. (2012). Transcriptional co-regulation of neuronal migration and laminar identity in the neocortex. Development 139, 1535-1546. doi: 10.1242/dev.069963
77. Laurie, D. J., Wisden, W., and Seeburg, P. H. (1992). The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J. Neurosci. 12, 4151-4172.
78. Lee, S., Yoon, B. E., Berglund, K., Oh, S. J., Park, H., Shin, H. S., et al. (2010). Channel-Mediated tonic GABA release from Glia. Science 330, 790-796. doi: 10.1126/science.1184334
79. Le Magueresse, C., Alfonso, J., Bark, C., Eliava, M., Khrulev, S., and Monyer, H. (2012). Subventricular zone-derived neuroblasts use vasculature as a scaffold to migrate radially to the cortex in neonatal mice. Cereb. Cortex 22, 2285-2296. doi: 10.1093/cercor/bhr302
80. Letinic, K., Zoncu, R., and Rakic, P. (2002). Origin of GABAergic neurons in the human neocortex. Nature 417, 645-649. doi: 10.1038/nature00779
81. Lobo, I. A., and Harris, R. A. (2008). GABA-A receptors and alcohol. Pharmacol. Biochem. Behav. 90, 90-94. doi: 10.1016/j.pbb.2008.03.006
82. Lopez-Bendito, G., Lujan, R., Shigemoto, R., Ganter, P., Paulsen, O., and Molnar, Z. (2003). Blockade ofGABA-B receptors alters the tangential migration ofcortical neurons. Cereb. Cortex 13, 932-942. doi: 10.1093/cercor/13.9.932
83. Lopez-Bendito, G., Shigemoto, R., Fairen, A., and Lujan, R. (2002a). Differential distribution of group I metabotropic glutamate receptors during rat cortical development. Cereb. Cortex 12, 625-638. doi: 10.1093/cercor/12.6.625
84. Lopez-Bendito, G., Shigemoto, R., Kulik, A., Paulsen, O., Fairen, A., and Lujan, R. (2002b). Expression and distribution of metabotropic GABA receptor subtypes GABA-BR1 and GABA-BR2 during rat neocortical development. Eur. J. Neurosci. 15, 1766-1778. doi: 10.1046/j.1460-9568.2002.02032.x
85. LoTurco, J. J., and Bai, J. (2006). The multipolar stage and disruptions in neuronal migration. Trends Neurosci. 29, 407-413. doi: 10.1016/j.tins.2006.05.006
86. LoTurco, J. J., Owens, D. F., Heath, M. J. S., Davis, M. B. E., and Kriegstein, A. R. (1995). GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15, 1287-1298. doi: 10.1016/0896-6273(95)90008-x
87. Luhmann, H. J., Kirischuk, S., Sinning, A., and Kilb, W. (2014). Early GABAergic circuitryin the cerebral cortex. Curr. Opin. Neurobiol. 26, 72-78. doi: 10.1016/j.conb.2013.12.014
88. Lujan, R., Shigemoto, R., and Lopez-Bendito, G. (2005). Glutamate and GABA receptor signalling in the developing brain. Neuroscience 130, 567-580. doi: 10.1016/j.neuroscience.2004.09.042
89. Ma, T., Wang, C. M., Wang, L., Zhou, X., Tian, M., Zhang, Q. Q., et al. (2013). Subcortical origins of human and monkey neocortical interneurons. Nat. Neurosci. 16, 1588-1597. doi: 10.1038/nn.3536
90. Mancini, J. D., and Atchison, W. D. (2007). The NR2B subunit in NMDA receptors is functionally important during cerebellar granule cell migration. Neurosci. Lett. 429, 87-90. doi: 10.1016/j.neulet.2007.09.079
91. Manent, J. B., Beguin, S., Ganay, T., and Represa, A. (2011). Cell-autonomous and cell-to-cell signalling events in normal and altered neuronal migration. Eur. J. Neurosci. 34, 1595-1608. doi: 10.1111/j.1460-9568.2011.07867.x
92. Manent, J. B., Demarque, M., Jorquera, I., Pellegrino, C., Ben-Ari, Y., Aniksztejn, L., et al. (2005). A noncanonical release of GABA and glutamate modulates neuronal migration. J. Neurosci. 25, 4755-4765. doi: 10.1523/jneurosci.0553-05.2005
93. Manent, J. B., Jorquera, I., Ben-Ari, Y., Aniksztejn, L., and Represa, A. (2006). Glutamate acting on AMPA but not NMDA receptors modulates the migration of hippocampal interneurons. J. Neurosci. 26, 5901-5909. doi: 10.1523/jneurosci.1033-06.2006
94. Manent, J. B., Jorquera, I., Mazzucchelli, I., Depaulis, A., Perucca, E., Ben-Ari, Y., et al. (2007). Fetal exposure to GABA-acting antiepileptic drugs generates hippocampal and cortical dysplasias. Epilepsia 48, 684-693. doi: 10.1111/j.1528-1167.2007.01056.x
95. Manent, J. B., and Represa, A. (2007). Neurotransmitters and brain maturation: early paracrine actions of GABA and glutamate modulate neuronal migration. Neuroscientist 13, 268-279. doi: 10.1177/1073858406298918
96. Marin, O. (2013). Cellular and molecular mechanisms controlling the migration of neocortical interneurons. Eur. J. Neurosci. 38, 2019-2029. doi: 10.1111/ejn.12225
97. Marret, S., Gressens, P., and Evrard, P. (1996). Arrest of neuronal migration by excitatoryamino acids in hamster developing brain. Proc. Natl. Acad. Sci. U S A 93, 15463-15468. doi: 10.1073/pnas.93.26.15463
98. Maskos, U., and McKay, R. D. G. (2003). Neural cells without functional N-methyl-D-aspartate (NMDA) receptors contribute extensivelyto normal postnatal brain development in efficiently generated chimaeric NMDA R1-/-<->+/+ mice. Dev. Biol. 262, 119-136. doi: 10.1016/s0012-1606(03)00354-3
99. Messersmith, E. K., Feller, M. B., Zhang, H., and Shatz, C. J. (1997). Migration of neocortical neurons in the absence of functional NMDA receptors. Mol. Cell. Neurosci. 9, 347-357. doi: 10.1006/mcne.1997.0646
100. Miller, M. W. (1992). "Effects of prenatal exposure to ethanol on cell proliferation and neuronal migration," in Development ofthe Centarl Nervous System, ed M. W. Miller (New York, Chichester, Brisbane, Toronto, Singapore: John Wiley and Sons, Inc.), 47-69.
101. Morishima, T., Uematsu, M., Furukawa, T., Yanagawa, Y., Fukuda, A., and Yoshida, S. (2010). GABA imaging in brain slices using immobilized enzyme-linked photoanalysis. Neurosci. Res. 67, 347-353. doi: 10.1016/j.neures.2010.04.005
102. Moya, F., and Valdeolmillos, M. (2004). Polarized increase of calcium and nucleokinesis in tangentially migrating neurons. Cereb. Cortex 14, 610-618. doi: 10.1093/cercor/bhh022
103. Nadarajah, B., Alifragis, P., Wong, R. O. L., and Parnavelas, J. G. (2003). Neuronal migration in the developing cerebral cortex: observations based on real-time imaging. Cereb. Cortex 13, 607-611. doi: 10.1093/cercor/13.6.607
104. Nimmervoll, B., Denter, D. G., Sava, I., Kilb, W., and Luhmann, H. J. (2011). Glycine receptors influence radial migration in the embryonic mouse neocortex. Neuroreport 22, 509-513. doi: 10.1097/wnr.0b013e328348aafe
105. Noctor, S. C., Flint, A. C., Weissman, T. A., Dammerman, R. S., and Kriegstein, A. R. (2001). Neurons derived from radial glial cells establish radial units in neocortex. Nature 409, 714-720. doi: 10.1038/35055553
106. Noctor, S. C., Martinez-Cerdeno, V., Ivic, L., and Kriegstein, A. R. (2004). Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7, 136-144. doi: 10.1038/nn1172
107. Okabe, A., Kilb, W., Shimizu-Okabe, C., Hanganu, I. L., Fukuda, A., and Luhmann, H. J. (2004). Homogenous glycine receptor expression in cortical plate neurons and Cajal-Retzius cells of neonatal rat cerebral cortex. Neuroscience 123, 715-724. doi: 10.1016/j.neuroscience.2003.10.014
108. Owens, D. F., Liu, X. L., and Kriegstein, A. R. (1999). Changing properties of GABAA receptor-mediated signaling during early neocortical development. J. Neurophysiol. 82, 570-583.
109. Pla, R., Borrell, V., Flames, N., and Marin, O. (2006). Layer acquisition by cortical GABAergic interneurons is independent of Reelin signaling. J. Neurosci. 26, 6924-6934. doi: 10.1523/jneurosci.0245-06.2006
110. Poluch, S., and Konig, N. (2002). AMPA receptor activation induces GABA release from neurons migrating tangentially in the intermediate zone of embryonic rat neocortex. Eur. J. Neurosci. 16, 350-354. doi: 10.1046/j.1460-9568.2002.02068.x
111. Qian, T. Z., Chen, R. Q., Nakamura, M., Furukawa, T., Kumada, T., Akita, T., et al. (2014). Activity-dependent endogenous taurine release facilitates excitatory neurotransmission in the neocortical marginal zone ofneonatal rats. Front. Cell. Neurosci. 8:33. doi: 10.3389/fncel.2014.00033
112. Rakic, P. (1972). Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neurol. 145, 61-83. doi: 10.1002/cne.901450105
113. Rakic, P. (2009). Evolution of the neocortex: a perspective from developmental biology. Nat. Rev. Neurosci. 10, 724-735. doi: 10.1038/nrn2719
114. Reiprich, P., Kilb, W., and Luhmann, H. J. (2005). Neonatal NMDA receptor blockade disturbs neuronal migration in rat somatosensory cortex in vivo. Cereb. Cortex 15, 349-358. doi: 10.1093/cercor/bhh137
115. Riccio, O., Jacobshagen, M., Golding, B., Vutskits, L., Jabaudon, D., Hornung, J.P., et al. (2011). Excess of serotonin affects neocortical pyramidal neuron migration. Transl. Psychiat. 1:e47. doi: 10.1038/tp.2011.49
116. Senturk, A., Pfennig, S., Weiss, A., Burk, K., and Acker-Palmer, A. (2011). Ephrin Bs are essential components ofthe Reelin pathway to regulate neuronal migration. Nature 472, 356-360. doi: 10.1038/nature09874
117. Smith, A. L., Cordery, P. M., and Thompson, I. D. (1995). Manufacture and release characteristics of Elvax polymers containing glutamate receptor antagonists. J. Neurosci. Methods 60, 211-217. doi: 10.1016/0165-0270(95)00014-l
118. Soria, J. M., and Valdeolmillos, M. (2002). Receptor-activated calcium signals in tangentially migrating cortical cells. Cereb. Cortex 12, 831-839. doi: 10.1093/cercor/12.8.831
119. Sykova, E. (2004). Extrasynaptic volume transmission and diffusion parameters of the extracellular space. Neuroscience 129, 861-876. doi: 10.1016/j.neuroscience.2004.06.077
120. Takano, T., Sawai, C., and Takeuchi, Y. (2004). Radial and tangential neuronal migration disorder in ibotenate-induced cortical lesions in hamsters: immunohistochemical study of reelin, vimentin and calretinin. J. Child Neurol. 19, 107-115. doi: 10.1177/08830738040190020501
121. Tanaka, D. H., and Nakajima, K. (2012). Migratory pathways of GABAergic interneurons when they enter the neocortex. Eur. J. Neurosci. 35, 1655-1660. doi: 10.1111/j.1460-9568.2012.08111.x
122. Tanaka, D., Nakaya, Y., Yanagawa, Y., Obata, K., and Murakami, F. (2003). Multimodal tangential migration of neocortical GABAergic neurons independent of GPI-anchored proteins. Development 130, 5803-5813. doi: 10.1242/dev.00825
123. Tanaka, D. H., Yanagida, M., Zhu, Y., Mikami, S., Nagasawa, T., Miyazaki, J., et al. (2009). Random walk behavior of migrating cortical interneurons in the marginal zone: time-lapse analysis in flat-mount cortex. J. Neurosci. 29, 1300-1311. doi: 10.1523/jneurosci.5446-08.2009
124. Tarnok, K., Czondor, K., Jelitai, M., Czirok, A., and Schlett, K. (2008). NMDA receptor NR2B subunit over-expression increases cerebellar granule cell migratory activity. J. Neurochem. 104, 818-829. doi: 10.1111/j.1471-4159.2007.0501.x
125. Teissier, A., Griveau, A., Vigier, L., Piolot, T., Borello, U., and Pierani, A. (2010). A novel transient glutamatergic population migrating from the pallial-subpallial boundarycontributes to neocortical development. J. Neurosci. 30, 10563-10574. doi: 10.1523/jneurosci.0776-10.2010
126. Thomas, C. G., Tian, H., and Diamond, J. S. (2011). The relative roles of diffusion and uptake in clearing synaptically released glutamate change during early postnatal development. J. Neurosci. 31, 4743-4754. doi: 10.1523/jneurosci.5953-10.2011
127. Ulrich, D., and Bettler, B. (2007). GABA(B) receptors: synaptic functions and mechanisms of diversity. Curr. Opin. Neurobiol. 17, 298-303. doi: 10.1016/j.conb.2007.04.001
128. Unichenko, P., Dvorzhak, A., and Kirischuk, S. (2013). Transporter-mediated replacement of extracellular glutamate for GABA in the developing murine neocortex. Eur. J. Neurosci. 38, 3580-3588. doi: 10.1111/ejn.12380
129. Valiente, M., and Marin, O. (2010). Neuronal migration mechanisms in development and disease. Curr. Opin. Neurobiol. 20, 68-78. doi: 10.1016/j.conb.2009.12.003
130. Wang, Y., Dye, C. A., Sohal, V., Long, J. E., Estrada, R. C., Roztocil, T., et al. (2010). Dlx5 and Dlx6 regulate the development of parvalbumin-expressing cortical interneurons. J. Neurosci. 30, 5334-5345. doi: 10.1523/jneurosci.5963-09.2010
131. Wang, T. Y., Kumada, T., Morishima, T., Iwata, S., Kaneko, T., Yanagawa, Y., et al. (2014). Accumulation of GABAergic Neurons, causing a focal ambient GABA gradient and downregulation of KCC2 are induced during microgyrus formation in a mouse model of polymicrogyria. Cereb. Cortex 24, 1088-1101.doi: 10.1093/cercor/bhs375
132. Won, C., Lin, Z. C., Kumar, T. P., Li, S. Y., Ding, L., Elkhal, A., et al. (2013). Autonomous vascular networks synchronize GABA neuron migration in the embryonic forebrain. Nat. Comm. 4:2149. doi: 10.1038/ncomms3149
133. Yamada, J., Okabe, A., Toyoda, H., Kilb, W., Luhmann, H. J., and Fukuda, A. (2004). Cl-uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated byNKCC1. J. Physiol. 557, 829-841. doi: 10.1113/jphysiol.2004.062471
134. Yu, Y. C., Bultje, R. S., Wang, X., and Shi, S. H. (2009). Specific synapses develop preferentially among sister excitatory neurons in the neocortex. Nature 458, 501-504. doi: 10.1038/nature07722
135. Zheng, J. Q., and Poo, M. M. (2007). Calcium signaling in neuronal motility. Annu. Rev. Cell Dev. Biol. 23, 375-404. doi: 10.1146/annurev.cellbio.23.090506.123221
136. Zimmer, G., Garcez, P., Rudolph, J., Niehage, R., Weth, F., Lent, R., et al. (2008). Ephrin-A5 acts as a repulsive cue for migrating cortical interneurons. Eur. J. Neurosci. 28, 62-73. doi: 10.1111/j.1460-9568.2008.06320.x