GABA receptor antagonists modulate postmitotic cell migration in slice cultures of embryonic rat cortex
Abstract
Recent studies indicate that GABA acts as a chemoattractant during rat cortical histogenesis. In vivo, GABA localizes in appropriate locations for a chemoattractant, along migratory routes and near target destinations for migrating cortical neurons. In vitro, GABA induces dissociated embryonic cortical neurons to migrate. Here, embryonic rat cortical slices were cultured in the presence or absence of GABA receptor (GABA-R) antagonists to assess GABA's effects on neuronal migration in situ. Gestational day 18 (E18) cortical slices were incubated overnight in bromodeoxyuridine (BrdU)-containing medium to label ventricular zone (vz) cells as they underwent terminal mitosis. The slices were then cultured in BrdU-free medium with or without GABA-R antagonists. In control slices, most BrdU(+) cells were observed in the cortical plate (cp) after 48 h. In contrast, cultures maintained in either saclofen (a GABA(B)-R antagonist) or picrotoxin (a GABA(A/C)-R antagonist) had few BrdU-labeled cp cells. However, the effects of the two antagonists were distinct. In the picrotoxin-treated slices, nearly half of all BrdU(+) cells remained in the vz and subventricular zone (svz), whereas saclofen treatment resulted in an accumulation of BrdU(+) cells in the intermediate zone (iz). Bicuculline, a GABA(A)-R antagonist, did not block, but rather enhanced migration of BrdU(+) cells into the cp. These results provide evidence that picrotoxin-sensitive receptors promote the migration of vz/svz cells into the iz, while saclofen-sensitive receptors signal cells to migrate into the cp. Thus, as cortical cells differentiate, changing receptor expression appears to modulate migratory responses to GABA.
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GABA influences neuronal migration in the embryonic cortex, interneuron settlement in the cortical plate, inhibitory synapse formation, and may influence pyramidal cell neurogenesis.
“GABA has been shown to influence neuronal migration in the embryonic cortex (Behar et al., 2000; López-Bendito et al., 2003), the settlement of interneurons in the cortical plate (Bortone and Polleux, 2009), and the formation on inhibitory synapses (Oh et al., 2016), and may also influence the neurogenesis of pyramidal cells (Silva et al., 2018).”
From Development and Functional Diversification of Cortical Interneurons (2018) · cites this paper as Behar et al., 2000
Cites
Mode of cell migration to the superficial layers of fetal monkey neocortex
Rakic, P. (1972) · Journal of Comparative Neurology · doi:10.1002/cne.901450105 · Cited by 2,170 · see citing works
Modulation of Neuronal Migration by NMDA Receptors
Komuro, H., & RAKIC, P. T. (1993) · Science · doi:10.1126/science.8096653 · Cited by 1,041 · see citing works
Principles of neural cell migration
RAKIC, P. T. (1990) · Cellular and Molecular Life Sciences · doi:10.1007/bf01939380 · Cited by 653 · see citing works
Ui, M. (1984) · Trends in Pharmacological Sciences · doi:10.1016/0165-6147(84)90444-9 · Cited by 566 · see citing works
GABA receptor mechanisms in the central nervous system
Sivilotti, L. G., & Nistri, A. (1991) · Progress in Neurobiology · doi:10.1016/0301-0082(91)90036-z · Cited by 554 · see citing works
In vivo regulation of axon extension and pathfinding by growth-cone calcium transients
Gómez, T. M., & Spitzer, N. C. (1999) · Nature · doi:10.1038/16927 · Cited by 483 · see citing works
A role for Cajal–Retzius cells and reelin in the development of hippocampal connections
Del Río, J. A., Heimrich, B., Borrell, V., Förster, E., Drakew, A., Alcántara, S., Nakajima, K., Miyata, T., Ogawa, M., Mikoshiba, K., et al. (1997) · Nature · doi:10.1038/385070a0 · Cited by 472 · see citing works
Diverse Migratory Pathways tn the Developing Cerebral Cortex
O’Rourke, N. A., Dailey, M. E., Smith, S. J., & McConnell, S. K. (1992) · Science · doi:10.1126/science.1411527 · Cited by 458 · see citing works
Hatten, M. E. (1990) · Trends in Neurosciences · doi:10.1016/0166-2236(90)90044-b · Cited by 448 · see citing works
Nestin expression in embryonic human neuroepithelium and in human neuroepithelial tumor cells.
Tohyama, T., Lee, V. M., RORKE, L. B., Marvin, M. J., McKay, R. D. G., & Trojanowski, J. Q. (1992) · PubMed · Cited by 412 · see citing works
Prenatal ontogeny of the gabaergic system in the rat brain: An immunocytochemical study
Lauder, J. M., Han, V. K. M., Henderson, P., Verdoorn, T. A., & Towle, A. C. (1986) · Neuroscience · doi:10.1016/0306-4522(86)90275-7 · Cited by 385 · see citing works
Behar, T. N., Li, Y., Tran, H., Ma, W., Dunlap, V., Scott, C., & Barker, J. L. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-05-01808.1996 · Cited by 379 · see citing works
Pharmacology of GABA receptor CI− channels in rat retinal bipolar cells
Feigenspan, A., Wässle, H., & Bormann, J. (1993) · Nature · doi:10.1038/361159a0 · Cited by 352 · see citing works
Markers for neuronal degeneration in organotypic slice cultures
Noraberg, J., Kristensen, B. W., & Zimmer, J. (1999) · Brain Research Protocols · doi:10.1016/s1385-299x(98)00050-6 · Cited by 307 · see citing works
Tangential migration of neurons in the developing cerebral cortex
O’Rourke, N. A., Sullivan, D. P., Kaznowski, C. E., Jacobs, A. A., & McConnell, S. K. (1995) · Development · doi:10.1242/dev.121.7.2165 · Cited by 240 · see citing works
Differential Response of Cortical Plate and Ventricular Zone Cells to GABA as a Migration Stimulus
Behar, T. N., Schaffner, A. E., Scott, C. A., O'Connell, C. L., & Barker, J. L. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-16-06378.1998 · Cited by 216 · see citing works
Ca2 channel‐regulated neuronal gene expression
Finkbeiner, S. M., & Greenberg, M. E. (1998) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(199810)37:1 · Cited by 202 · see citing works
Hunter, K. E., & Hatten, M. E. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.6.2061 · Cited by 167 · see citing works
Gomez, T. M., Snow, D. M., & Letourneau, P. C. (1995) · Neuron · doi:10.1016/0896-6273(95)90270-8 · Cited by 142 · see citing works
Differential survival of Cajal-Retzius cells in organotypic cultures of hippocampus and neocortex
Del Rı́o, J. A., Heimrich, B., Supèr, H., Borrell, V., Frotscher, M., & Soriano, E. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-21-06896.1996 · Cited by 133 · see citing works
A novel model of glioma cell invasion using organotypic brain slice culture.
Ohnishi, T., Matsumura, H., Izumoto, S., Hiraga, S., & Hayakawa, T. (1998) · PubMed · Cited by 123 · see citing works
Ma, W., & Barker, J. L. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-03-02547.1995 · Cited by 102 · see citing works
Formation and preservation of cortical layers in slice cultures
Götz, M., & Bolz, J. (1992) · Journal of Neurobiology · doi:10.1002/neu.480230702 · Cited by 97 · see citing works
Cellular organization and development of slice cultures from rat visual cortex
Caeser, M., Bonhoeffer, T., & Bolz, J. (1989) · Experimental Brain Research · doi:10.1007/bf00274981 · Cited by 92 · see citing works
Neurotrophins Stimulate Chemotaxis of Embryonic Cortical Neurons
Behar, T. N., Dugich‐Djordjevic, M. M., Li, Y., Ma, W., Somogyi, R., Wen, X., Brown, E. R., Scott, C., McKay, R. D. G., & Barker, J. L. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01685.x · Cited by 92 · see citing works
Kerr, D. I. B., & Ong, J. A. (1992) · Medicinal Research Reviews · doi:10.1002/med.2610120604 · Cited by 85 · see citing works
Dantzker, J. L. M., & Callaway, E. M. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-11-04145.1998 · Cited by 83 · see citing works
Lavdas, A. Α., Blue, M. E., Lincoln, J., & Parnavelas, J. G. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-20-07872.1997 · Cited by 80 · see citing works
Role of apolipoprotein E and estrogen in mossy fiber sprouting in hippocampal slice cultures
Teter, B., Harris‐White, M. E., Frautschy, S. A., & Cole, G. M. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00630-7 · Cited by 71 · see citing works
Development of the lateral and medial limbic cortices in the rat in relation to cortical phylogeny
Bayer, S. A. (1990) · Experimental Neurology · doi:10.1016/0014-4886(90)90150-q · Cited by 66 · see citing works
Klostermann, O., & Wahle, P. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00009-3 · Cited by 63 · see citing works
Total number of neurons in the layers of the human entorhinal cortex
West, M. J., & Slomianka, L. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1998)8:1 · Cited by 57 · see citing works
Cell Migration in Cultured Cerebral Cortical Slices
Roberts, J. S., O’Rourke, N. A., & McConnell, S. K. (1993) · Developmental Biology · doi:10.1006/dbio.1993.1038 · Cited by 55 · see citing works
Zhang, J., Shen, W., & Slaughter, M. M. (1997) · The Journal of General Physiology · doi:10.1085/jgp.110.1.45 · Cited by 55 · see citing works
Migration of granule neurons in cerebellar organotypic cultures is impaired by methylmercury
Kunimoto, M., & Suzuki, T. (1997) · Neuroscience Letters · doi:10.1016/s0304-3940(97)00273-5 · Cited by 53 · see citing works
Cajal-Retzius neurons identified by GABA immunohistochemistry in layer I of the rat cerebral cortex
Imamoto, K., Karasawa, N., Isomura, G., & Nagatsu, I. (1994) · Neuroscience Research · doi:10.1016/0168-0102(94)90027-2 · Cited by 48 · see citing works
Weisenhorn, D. M. V., Celio, M. R., & Rickmann, M. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00120.x · Cited by 39 · see citing works
Meningeal cells stimulate and direct the migration of cerebellar external granule cells in vitro
Hartmann, D., Schulze, M., & Sievers, J. (1998) · Journal of Neurocytology · doi:10.1023/a:1006998609999 · Cited by 32 · see citing works
G Protein-Mediated Inhibition of Neuronal Migration Requires Calcium Influx
Horgan, A., & Copenhaver, P. F. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-11-04189.1998 · Cited by 30 · see citing works
Arimatsu, Y., & Ishida, M. (1998) · Developmental Brain Research · doi:10.1016/s0165-3806(97)00197-1 · Cited by 30 · see citing works
Baratta, J. L., Marienhagen, J., Ha, D. H., Yu, J., & Robertson, R. T. (1996) · Neuroscience · doi:10.1016/0306-4522(95)00603-6 · Cited by 21 · see citing works
A receptor with GABAC-like pharmacology in invertebrate neurones in culture
Jackel, C., Krenz, W. D., & Nagy, F. (1994) · Neuroreport · doi:10.1097/00001756-199405000-00019 · Cited by 17 · see citing works
Yoshikawa, M., Goto, S., Okamura, A., Hamasaki, T., & Ushio, Y. (1998) · Acta Neuropathologica · doi:10.1007/s004010050845 · Cited by 12 · see citing works
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GABA: A Pioneer Transmitter That Excites Immature Neurons and Generates Primitive Oscillations
Ben-Ari, Y., Gaiarsa, J.-L., Tyzio, R., & Khazipov, R. (2007) · Physiological Reviews · doi:10.1152/physrev.00017.2006 · Cited by 1,304 · see citing works
Is there more to gaba than synaptic inhibition?
Owens, D. F., & Kriegstein, A. R. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn919 · Cited by 1,158 · see citing works
C ELL M IGRATION IN THE F OREBRAIN
Marín, Ó., & Rubenstein, J. L. R. (2003) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.041002.131058 · Cited by 917 · see citing works
Development and Functional Diversification of Cortical Interneurons
Lim, L., Mi, D., Llorca, A., & Marín, O. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.009 · Cited by 714 · see citing works
“Are some of the transient interneurons important for shaping early neuronal networks, similar to Cajal-Retzius cells? GABA has been shown to influence neuronal migration in the embryonic cortex (Behar et al., 2000; López-Bendito et al., 2003), the settlement of interneurons in the cortical plate (Bortone and Polleux,…”
Wichterle, H., Turnbull, D. H., Nery, S., Fishell, G., & Alvarez-Buylla, A. (2001) · Development · doi:10.1242/dev.128.19.3759 · Cited by 722 · see citing works
Trekking across the Brain: The Journey of Neuronal Migration
Ayala, R., Shu, T., & Tsai, L.-H. (2007) · Cell · doi:10.1016/j.cell.2006.12.021 · Cited by 620 · see citing works
GABAergic Interneurons Shape the Functional Maturation of the Cortex
Le Magueresse, C., & Monyer, H. (2013) · Neuron · doi:10.1016/j.neuron.2013.01.011 · Cited by 425 · see citing works
Glutamate and GABA receptor signalling in the developing brain
Luján, R., Shigemoto, R., & López‐Bendito, G. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.09.042 · Cited by 409 · see citing works
Moody, W. J., & Bosma, M. M. (2005) · Physiological Reviews · doi:10.1152/physrev.00017.2004 · Cited by 394 · see citing works
Excitatory GABA Action Is Essential for Morphological Maturation of Cortical Neurons <i>In Vivo</i>
Cancedda, L., Fiumelli, H., Chen, K., & Poo, M.-M. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5169-06.2007 · Cited by 392 · see citing works
Neurotransmitters as early signals for central nervous system development
Nguyen, L., Rigo, J., Rocher, V., Belachew, S. M., Malgrange, B., Rogister, B., Leprince, P., & Moonen, G. (2001) · Cell and Tissue Research · doi:10.1007/s004410000343 · Cited by 371 · see citing works
Prenatal exposure to drugs: effects on brain development and implications for policy and education
Thompson, B. L., Levitt, P. R., & Stanwood, G. D. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2598 · Cited by 367 · see citing works
GABA sets the tempo for activity-dependent adult neurogenesis
Ge, S., Pradhan, D. A., Ming, G., & Song, H. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.11.001 · Cited by 366 · see citing works
Defining the role of GABA in cortical development
Wang, D. D., & Kriegstein, A. R. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2008.167635 · Cited by 336 · see citing works
Chattopadhyaya, B., Cristo, G. D., Wu, C. Z., Knott, G. W., Kuhlman, S. J., Fu, Y., Palmiter, R. D., & Huang, Z. J. (2007) · Neuron · doi:10.1016/j.neuron.2007.05.015 · Cited by 326 · see citing works
Calcium Signaling in Neuronal Motility
Zheng, J. Q., & Poo, M.-M. (2007) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.23.090506.123221 · Cited by 292 · see citing works
Neurodevelopment, GABA System Dysfunction, and Schizophrenia
Schmidt, M. J., & Mirnics, K. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.95 · Cited by 239 · see citing works
A Noncanonical Release of GABA and Glutamate Modulates Neuronal Migration
Manent, J.-B., Demarque, M., Jorquera, I., Pellegrino, C., Ben-Ari, Y., Aniksztejn, L., & Represa, A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0553-05.2005 · Cited by 220 · see citing works
Iguchi, T., Sakata, K., Yoshizaki, K., Tago, K., Mizuno, N., & Itoh, H. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m708919200 · Cited by 195 · see citing works
Development of the GABAergic System from Birth to Adolescence
Kilb, W. (2012) · The Neuroscientist · doi:10.1177/1073858411422114 · Cited by 190 · see citing works
Wang, D. D., Krueger‐Burg, D., & Bordey, A. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.042572 · Cited by 189 · see citing works
Functions and Regulatory Mechanisms of Gq-Signaling Pathways
Mizuno, N., & Itoh, H. (2009) · Neurosignals · doi:10.1159/000186689 · Cited by 181 · see citing works
Fragile X Syndrome: The GABAergic System and Circuit Dysfunction
Paluszkiewicz, S. M., Martin, B. S., & Huntsman, M. M. (2011) · Developmental Neuroscience · doi:10.1159/000329420 · Cited by 177 · see citing works
The postnatal GABA shift: A developmental perspective
Peerboom, C., & Wierenga, C. J. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.01.024 · Cited by 174 · see citing works
GABAergic excitation after febrile seizures induces ectopic granule cells and adult epilepsy
Koyama, R., Tao, K., Sasaki, T., Ichikawa, J., Miyamoto, D., Muramatsu, R., Matsuki, N., & Ikegaya, Y. (2012) · Nature Medicine · doi:10.1038/nm.2850 · Cited by 174 · see citing works
Obrietan, K. H., Gao, X., & van den Pol, A. N. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.88.2.1005 · Cited by 167 · see citing works
Control of cortical neuronal migration by glutamate and GABA
Luhmann, H. J., Fukuda, A., & Kilb, W. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00004 · Cited by 167 · see citing works
Maric, D., Liu, Q., Marić, I., Chaudry, S., Chang, Y.-H., Smith, S. V., Sieghart, W., Fritschy, J., & Barker, J. L. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-07-02343.2001 · Cited by 156 · see citing works
GABA signalling during development: new data and old questions
Varjú, P., Katarova, Z., Madarász, E., & Szabó, G. (2001) · Cell and Tissue Research · doi:10.1007/s004410100356 · Cited by 143 · see citing works
Blockade of GABAB Receptors Alters the Tangential Migration of Cortical Neurons
Lopez-Bendito, G. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.9.932 · Cited by 136 · see citing works
Carlson, V. C. C., Yeh, P. W. L., Yanagawa, Y., Obata, K., & Yeh, H. H. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5110-07.2008 · Cited by 140 · see citing works
Development of the ventromedial nucleus of the hypothalamus
McClellan, K., Parker, K. L., & Tobet, S. A. (2006) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2006.02.002 · Cited by 139 · see citing works
GABA-A Receptors Regulate Neocortical Neuronal Migration In Vitro and In Vivo
Heck, N., Kilb, W., Reiprich, P., Kubota, H., Furukawa, T., Fukuda, A., & Luhmann, H. J. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhj135 · Cited by 136 · see citing works
Manent, J., & Represa, A. (2007) · The Neuroscientist · doi:10.1177/1073858406298918 · Cited by 131 · see citing works
GABAB Receptors Mediate Motility Signals for Migrating Embryonic Cortical Cells
Behar, T. N. (2001) · Cerebral Cortex · doi:10.1093/cercor/11.8.744 · Cited by 130 · see citing works
Electrical activity patterns and the functional maturation of the neocortex
Kilb, W., Kirischuk, S., & Luhmann, H. J. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07878.x · Cited by 124 · see citing works
Spatiotemporal specificity of GABAA receptor-mediated regulation of adult hippocampal neurogenesis
Duveau, V., Laustela, S., Barth, L., Gianolini, F., Vogt, K. E., Keist, R., Chandra, D., Homanics, G. E., Rudolph, U., & Fritschy, J. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07782.x · Cited by 121 · see citing works
Fetal Exposure to GABA‐Acting Antiepileptic Drugs Generates Hippocampal and Cortical Dysplasias
Manent, J., Jorquera, I., Mazzucchelli, I., Depaulis, A., Perucca, E., Ben‐Ari, Y., & Represa, A. (2007) · Epilepsia · doi:10.1111/j.1528-1167.2007.01056.x · Cited by 115 · see citing works
López‐Bendito, G., Shigemoto, R., Kulik, Á., Paulsen, O., Fairén, A. G., & Luján, R. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02032.x · Cited by 113 · see citing works
Glutamate Acting on AMPA But Not NMDA Receptors Modulates the Migration of Hippocampal Interneurons
Manent, J.-B., Jorquera, I., Ben-Ari, Y., Aniksztejn, L., & Represa, A. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1033-06.2006 · Cited by 112 · see citing works
Carlson, V. C. C., Yeh, P. W. L., Cheng, Q., & Yeh, H. H. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhj084 · Cited by 109 · see citing works
Autonomous vascular networks synchronize GABA neuron migration in the embryonic forebrain
Won, C., Lin, Z., Pandit, P. K. T., Li, S., Ding, L., Elkhal, A., Szabó, G., & Vasudevan, A. (2013) · Nature Communications · doi:10.1038/ncomms3149 · Cited by 104 · see citing works
Inoue, K., Furukawa, T., Kumada, T., Yamada, J., Wang, T., Inoue, R., & Fukuda, A. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.319418 · Cited by 99 · see citing works
Stewart, R. R., Hoge, G., Žigová, T., & Luskin, M. B. (2002) · Journal of Neurobiology · doi:10.1002/neu.10038 · Cited by 99 · see citing works
Functional role of ambient GABA in refining neuronal circuits early in postnatal development
Cellot, G., & Cherubini, E. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00136 · Cited by 96 · see citing works
Ageta‐Ishihara, N., Takemoto‐Kimura, S., Nonaka, M., Adachi-Morishima, A., Suzuki, K., Kamijo, S., Fujii, H., Mano, T., Blaeser, F., Chatila, T. A., et al. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3018-09.2009 · Cited by 93 · see citing works
Molecules and Mechanisms Involved in the Generation and Migration of Cortical Interneurons
Hernandez-Miranda, L. R., Parnavelas, J. G., & Chiara, F. (2010) · ASN NEURO · doi:10.1042/an20090053 · Cited by 90 · see citing works
The Early Fetal Development of Human Neocortical GABAergic Interneurons
Al‐Jaberi, N., Lindsay, S., Sarma, S., Bayatti, N., & Clowry, G. J. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht254 · Cited by 89 · see citing works
Seizures and Antiepileptic Drugs: Does Exposure Alter Normal Brain Development?
Marsh, E. D., Brooks‐Kayal, A. R., & Porter, B. E. (2006) · Epilepsia · doi:10.1111/j.1528-1167.2006.00894.x · Cited by 86 · see citing works
The importance of the excitatory amino acid transporter 3 (EAAT3)
Bjørn-Yoshimoto, W. E., & Underhill, S. M. (2016) · Neurochemistry International · doi:10.1016/j.neuint.2016.05.007 · Cited by 83 · see citing works
Neonatal NMDA Receptor Blockade Disturbs Neuronal Migration in Rat Somatosensory Cortex In Vivo
Reiprich, P. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh137 · Cited by 83 · see citing works
REVIEW ARTICLE: Neurotransmitters regulate cell migration in the telencephalon
Heng, J. I., Moonen, G., & Nguyen, L. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05694.x · Cited by 82 · see citing works
López‐Bendito, G., Shigemoto, R., Kulik, Á., Vida, I., Fairén, A., & Luján, R. (2004) · Hippocampus · doi:10.1002/hipo.10221 · Cited by 82 · see citing works
Bony, G., Szczurkowska, J., Tamagno, I., Shelly, M., Contestabile, A., & Cancedda, L. (2013) · Nature Communications · doi:10.1038/ncomms2820 · Cited by 81 · see citing works
GABAergic Regulation of Adult Hippocampal Neurogenesis
Sibbe, M., & Kulik, Á. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0072-3 · Cited by 81 · see citing works
Modulation of Neocortical Development by Early Neuronal Activity: Physiology and Pathophysiology
Kirischuk, S., Sinning, A., Blanquie, O., Yang, J., Luhmann, H. J., & Kilb, W. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00379 · Cited by 79 · see citing works
Gamma-aminobutyric acid (GABA) and cell proliferation: focus on cancer cells.
Watanabe, M., Maemura, K., Oki, K., Shiraishi, N., Shibayama, Y., & Katsu, K. (2006) · PubMed · doi:10.14670/hh-21.1135 · Cited by 79 · see citing works
Gago, N., El‐Etr, M., Sananès, N., Cadepond, F., Samuel, D., Avellana‐Adalid, V., Evercooren, A. B., & Schumacher, M. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20348 · Cited by 79 · see citing works
Role of tonic GABAergic currents during pre- and early postnatal rodent development
Kilb, W., Kirischuk, S., & Luhmann, H. J. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00139 · Cited by 78 · see citing works
Alcántara, S., Pozas, E., Ibañez, C. F., & Soriano, E. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhi128 · Cited by 71 · see citing works
Nipbl Interacts with Zfp609 and the Integrator Complex to Regulate Cortical Neuron Migration
van den Berg, D. L. C., Azzarelli, R., Oishi, K., Martynoga, B., Urbán, N., Dekkers, D. H. W., Demmers, J., & Guillemot, F. (2016) · Neuron · doi:10.1016/j.neuron.2016.11.047 · Cited by 72 · see citing works
Costa, L. G., Steardo, L., & Cuomo, V. (2004) · Pharmacological Reviews · doi:10.1124/pr.56.1.5 · Cited by 73 · see citing works
Tao, R., Davis, K. N., Li, C., Shin, J. H., Gao, Y., Jaffe, A. E., Gondré‐Lewis, M. C., Weinberger, D. R., Kleinman, J. E., & Hyde, T. M. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.105 · Cited by 72 · see citing works
Studer, R., von Boehmer, L., Haenggi, T., Schweizer, C., Benke, D., Rudolph, U., & Fritschy, J. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05006.x · Cited by 71 · see citing works
A Common Susceptibility Factor of Both Autism and Epilepsy: Functional Deficiency of GABAA Receptors
Kang, J., & Barnes, G. N. (2012) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-012-1543-7 · Cited by 70 · see citing works
Brain Sex Differences and Hormone Influences: A Moving Experience?
Tobet, S. A., Knoll, J. G., Hartshorn, C., Aurand, E. R., Stratton, M. S., Kumar, P., Searcy, B. T., & McClellan, K. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2009.01834.x · Cited by 68 · see citing works
GABAA Receptors, Anesthetics and Anticonvulsants in Brain Development
Henschel, O., Gipson, K. E., & Bordey, A. (2008) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/187152708784083812 · Cited by 70 · see citing works
Extracellular factors that regulate neuronal migration in the central nervous system
Sobeih, M. M., & Corfas, G. (2002) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(02)00040-0 · Cited by 67 · see citing works
Watanabe, M., Zhang, J., Mansuri, M. S., Duan, J., Karimy, J. K., Delpire, E. J., Alper, S. L., Lifton, R. P., Fukuda, A., & Kahle, K. T. (2019) · Science Signaling · doi:10.1126/scisignal.aaw9315 · Cited by 66 · see citing works
Luo, Y., Lathia, J. D., Mughal, M., & Mattson, M. P. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m800649200 · Cited by 65 · see citing works
Wilhelm, E. A., Jessé, C. R., Bortolatto, C. F., Nogueira, C. W., & Savegnago, L. (2009) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2009.03.006 · Cited by 65 · see citing works
Maddox, D. M., & Condie, B. G. (2001) · BMC Developmental Biology · doi:10.1186/1471-213x-1-1 · Cited by 64 · see citing works
Warm, D., Schroer, J., & Sinning, A. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.807969 · Cited by 60 · see citing works
Neurotransmitters and the Development of Neuronal Circuits
Ruediger, T., & Bolz, J. (2007) · Advances in Experimental Medicine and Biology · doi:10.1007/978-0-387-76715-4_8 · Cited by 62 · see citing works
Stanwood, G. D., Parlaman, J. P., & Levitt, P. R. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20548 · Cited by 62 · see citing works
Calcium signalling: a key regulator of neuronal migration
Horigane, S., Ozawa, Y., Yamada, H., & Takemoto‐Kimura, S. (2019) · The Journal of Biochemistry · doi:10.1093/jb/mvz012 · Cited by 60 · see citing works
Mulligan, M. K., Wang, X., Adler, A. L., Mozhui, K., Lu, L., & Williams, R. W. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034586 · Cited by 59 · see citing works
Li, Y.-H. (2012) · World Journal of Gastroenterology · doi:10.3748/wjg.v18.i21.2704 · Cited by 60 · see citing works
Calcium and activity-dependent signaling in the developing cerebral cortex
Arjun McKinney, A., Petrova, R., & Panagiotakos, G. (2022) · Development · doi:10.1242/dev.198853 · Cited by 55 · see citing works
Calcium signaling in neocortical development
Uhlén, P., Fritz, N., Smedler, E., Malmersjö, S., & Kanatani, S. (2015) · Developmental Neurobiology · doi:10.1002/dneu.22273 · Cited by 57 · see citing works
The role of neural activity in the migration and differentiation of enteric neuron precursors
Hao, M. M., moore, R. E., Roberts, R. R., Nguyen, T. V., Furness, J. B., Anderson, R. B., & Young, H. M. (2010) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2009.01462.x · Cited by 57 · see citing works
Emerging neurotrophic role of GABAB receptors in neuronal circuit development
Gaïarsa, J., & Porcher, C. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00206 · Cited by 57 · see citing works
Pozzi, D., Rasile, M., Corradini, I., & Matteoli, M. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-01027-6 · Cited by 55 · see citing works
Wolfe, C. A., Doren, M. V., Walker, H. J., Seney, M. L., McClellan, K., & Tobet, S. A. (2005) · Developmental Brain Research · doi:10.1016/j.devbrainres.2005.03.001 · Cited by 54 · see citing works
Autism: Neuropathology, Alterations of the GABAergic System, and Animal Models
van Kooten, I. A. J., Hof, P. R., van Engeland, H., Steinbusch, H. W. M., Patterson, P. H., & Schmitz, C. (2005) · International review of neurobiology · doi:10.1016/s0074-7742(05)71001-1 · Cited by 53 · see citing works
Pathophysiological power of improper tonic GABAA conductances in mature and immature models
Egawa, K., & Fukuda, A. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00170 · Cited by 54 · see citing works
Alcohol and the Developing Brain: Why Neurons Die and How Survivors Change
Granato, A., & Dering, B. R. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19102992 · Cited by 50 · see citing works
Denter, D. G., Heck, N., Riedemann, T., White, R., Kilb, W., & Luhmann, H. J. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.01.049 · Cited by 48 · see citing works
Liu, Y., Li, Y.-H., Guo, F., Wang, J., Sun, R., Hu, J., & Li, G. (2008) · World Journal of Gastroenterology · doi:10.3748/wjg.14.7175 · Cited by 47 · see citing works
Furukawa, T., Yamada, J., Akita, T., Matsushima, Y., Yanagawa, Y., & Fukuda, A. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00088 · Cited by 47 · see citing works
Raol, Y. H., Zhang, G., Budreck, E. C., & Brooks‐Kayal, A. R. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.01.005 · Cited by 45 · see citing works
Stimulation of TM3 Leydig cell proliferation via GABAA receptors: A new role for testicular GABA
Geigerseder, C., Doepner, R. F. G., Thalhammer, A., Krieger, A., & Mayerhofer, A. (2004) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-2-13 · Cited by 45 · see citing works
GABAergic signaling in the developing cerebellum
Takayama, C., & Inoue, Y. (2004) · Anatomical Science International · doi:10.1111/j.1447-073x.2004.00081.x · Cited by 44 · see citing works
Royland, J. E., & Kodavanti, P. R. S. (2008) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2008.04.023 · Cited by 44 · see citing works
Carlson, V. C. C., & Yeh, H. H. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq247 · Cited by 42 · see citing works
Westerholz, S., de Lima, A. D., & Voigt, T. B. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.03.039 · Cited by 41 · see citing works
Unichenko, P., Dvorzhak, A., & Kirischuk, S. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12380 · Cited by 41 · see citing works
GABA receptor ρ subunit expression in the developing rat brain
Alakuijala, A., Palgi, M., Wegelius, K., Schmidt, M., Enz, R., Paulin, L. G., Saarma, M., & Pasternack, M. (2004) · Developmental Brain Research · doi:10.1016/j.devbrainres.2004.09.010 · Cited by 41 · see citing works
Gomes, P., Bodo, C., Nogueras‐Ortiz, C. J., Samiotaki, M. K., Chen, M., Soares‐Cunha, C., Silva, J. M., Coimbra, B., Stamatakis, G. M., Santos, L. D. S., et al. (2023) · Cell Communication and Signaling · doi:10.1186/s12964-023-01045-z · Cited by 38 · see citing works
Hurni, N., Kolodziejczak, M., Tomasello, U., Badia, J., Jacobshagen, M., Prados, J., & Dayer, A. G. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx059 · Cited by 38 · see citing works
- Authors
- Behar, T. N.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Behar, T. N.
- Venue
- Cerebral Cortex
- Publisher
- Oxford University Press (OUP)
- Published
- 2000-09-01
- Volume
- 10
- Issue
- 9
- Pages
- 899-909
- ISSN
- 1047-3211 (ISSN-L)
- 1460-2199
- OpenAlex
- W2135435398
- Cited by
- 218
- References
- 43
- Citations by year
- 2025: 2 · 2024: 6 · 2023: 7 · 2022: 6 · 2021: 6 · 2020: 6 · 2019: 3 · 2018: 4 · 2017: 10 · 2016: 6 · 2015: 6 · 2014: 7 · 2013: 17 · 2012: 10
- FWCI
- 1.52
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cerebral Cortex (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Keywords
- GABA receptor antagonists, neuronal migration, picrotoxin, saclofen, bicuculline, GABAB receptors, GABAA receptor, GABAC receptors, ventricular zone, subventricular zone, intermediate zone, cortical plate, BrdU labeling
- MeSH terms
- Animals, Baclofen, Bicuculline, Bromodeoxyuridine, Cell Movement, Cerebral Cortex, Chemotaxis, Female, gamma-Aminobutyric Acid, Glial Fibrillary Acidic Protein, Intermediate Filament Proteins, Mitosis, Nerve Tissue Proteins, Neuroglia, Neurons, Organ Culture Techniques, Picrotoxin, Pregnancy, Receptors, GABA-A, Cellular Senescence, GABA Antagonists, Rats, Nestin
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