Changing properties of GABA(A) receptor-mediated signaling during early neocortical development

Journal of Neurophysiology

Volumn 82, Issue 2, 1999, Pages 570-583

  Owens, David F ^a   Liu, Xiaolin ^a   Kriegstein, Arnold R ^a  

^a Coll Phys Surgs of Columbia Univ ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN MATURATION; BRAIN REGION; CELL POPULATION; EMBRYO; GABAERGIC SYSTEM; INTERNEURON; NEOCORTEX; NONHUMAN; PRIORITY JOURNAL; RAT; STEM CELL; SYNAPSE;

EID: 0032769159     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1999.82.2.570     Document Type: Article

References (90)

1. AGMON, A., HOLLRIGEL, G., AND O'DOWD, D. K. Functional GABAergic synaptic connection in neonatal mouse barrel cortex. J. Neurosci. 16: 4684-4695, 1996.
2. AGMON, A. AND O'DOWD, D. K. NMDA-receptor-mediated currents are prominent in the thalamocortical synaptic response before maturation of inhibition. J. Neurophysiol. 68: 345-349, 1992.
3. A receptor inhibits the proliferative effects of bFGF in cortical progenitor cells. Eur. J. Neurosci. 9: 291-298, 1997.
4. A receptor subunit messenger RNAs show differential expression during cortical development in the rat brain. Neuroscience 51: 583-591, 1992.
5. BALSLEV, Y., SAUNDERS, N. R., AND MOLLGARD, K. Synaptogenesis in the neocortical anlage and early developing neocortex of rat embryos. Acta Anat. 156: 2-10, 1996.
6. A receptors in the outgrowth of cultured hippocampal neurons. Neurosci. Lett. 152: 150-154, 1993.
7. BARGMANN, C. I. Neurobiology of the Caenorhabditis elegans genome. Science 282: 2028-2033, 1998.
8. BEHAR, T. N., LI, Y., TRAN, H. T., MA, W., DUNLAP, V., SCOTT, C., AND BARKER, J. L. GABA stimulates chemotaxis and chemokinesis of embryonic cortical neurons via calcium-dependent mechanisms. J. Neurosci. 16: 1808-1818, 1996.
9. BEHAR, T. N., SCHAFFNER, A. E., SCOTT, C. A., O'CONNELL, C., AND BARKER, J. L. Differential response of cortical plate and ventricular zone cells to GABA as a migration stimulus. J. Neurosci. 18: 6378-6387, 1998.
10. BEN-ARI, Y., CHERUBINI, E., CORRADETTI, R., AND GAIARSA, J. L. Giant synaptic potentials in immature rat CA3 hippocampal neurones. J. Physiol. (Lond.) 416: 303-325, 1989.
11. BEN-ARI, Y., KHAZIPOV, R., LEINEKUGEL, X., CAILLARD, O., AND GAIARSA, J. L. GABAA, NMDA and AMPA receptors: a developmentally regulated "menage a trois." Trends Neurosci. 20: 523-529, 1997.
12. BERNINGER, B., MARTY, S., ZAFRA, F., DA PENHA BERZAGHI, M., AND THOENEN, H. GABAergic stimulation switches from enhancing to repressing BDNF expression in rat hippocampal neurons during maturation in vitro. Development 121: 2327-2335, 1995.
13. BITTMAN, K., OWENS, D. F., KRIEGSTEIN, A. R., AND LOTURCO, J. J. Cell coupling and uncoupling in the ventricular zone of developing neocortex. J. Neurosci. 17: 7037-7044, 1997.
14. BLANTON, M. G., LOTURCO, J. J., AND KRIEGSTEIN, A. R. Whole cell recording from neurons in slices of reptilian and mammalian cerebral cortex. J. Neurosci. Methods 30: 203-210, 1989.
15. B receptor subtypes. Trends Neurosci. 11: 112-116, 1988.
16. C receptors. Trends Neurosci. 18: 515-519, 1995.
17. BOURGEOIS, J. P. AND RAKIC, P. Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage. J. Neurosci. 13: 2801-2820, 1993.
18. A receptors. J. Physiol. (Lond.) 497: 3: 753-759, 1996.
19. BURGARD, E. C. AND HABLITZ, J. J. Developmental changes in NMDA and non-NMDA receptor-mediated synaptic potentials in rat neocortex. J. Neurophysiol. 69: 230-240, 1993a.
20. BURGARD, E. C. AND HABLITZ, J. J. NMDA receptor-mediated components of miniature excitatory synaptic currents in developing rat neocortex. J. Neurophysiol. 70: 1841-1852, 1993b.
21. CHEN, G., TROMBLEY, P. Q., AND VAN DEN POL, A. N. Excitatory actions of GABA in developing rat hypothalamic neurones. J. Physiol. (Lond.) 494: 451-464, 1996.
22. CHERUBINI, E., GAIARSA, J. L., AND BEN-ARI, Y. GABA: an excitatory transmitter in early postnatal life. Trends Neurosci. 14: 515-519, 1991.
23. CHERUBINI, E., ROVIRA, C., GAIARSA, J. L., CORRADETTI, R., AND BEN-ARI, Y. GABA mediated excitation in immature rat CA3 hippocampal neurons. Int. J. Dev. Neurosci. 8: 481-490, 1990.
24. - cotransporter expression in rat neocortex. Brain Res. Dev. Brain Res. 109: 281-292, 1998.
25. A receptor. Neuroscience 40: 375-397, 1991.
26. 2+ of rat cerebellar granule cells in expiant cultures. J. Neurosci. 7: 1384-1400, 1987.
27. B receptor-mediated responses in neocortex of rat and cat. J. Physiol. (Lond.) 406: 443-468, 1988.
28. A receptor subunit. Nature 385: 820-823, 1997.
29. DE FELIPE, J., MARCO, P., FAIREN, A., AND JONES, E. G. Inhibitory synaptogenesis in mouse somatosensory cortex. Cereb. Cortex 7: 619-634, 1997.
30. DURAND, G. M., KOVALCHUK, Y., AND KONNERTH, A. Long-term potentiation and functional synapse induction in developing hippocampus. Nature 381: 71-75, 1996.
31. A receptor subtypes requires the γ2 subunit and gephyrin. Nat. Neurosci. 1: 563-571, 1998.
32. FINNEY, E. M., STONE, J. R., AND SHATZ, C. J. Major glutamatergic projection from subplate into visual cortex during development. J. Comp. Neurol. 398: 105-118, 1998.
33. A-receptor subtypes during postnatal development: an immunohistochemical study. J. Neurosci. 14: 5302-5324, 1994.
34. FROSCH, M. P., LIPTON, S. A., AND DICHTER, M. A. Desensitization of GABA-activated currents and channels in cultured cortical neurons. J. Neurosci. 12: 3042-3053, 1992.
35. GAO, X. B., CHEN, G., AND VAN DEN POL, A. N. GABA-dependent firing of glutamate-evoked action potentials at AMPA/kainate receptors in developing hypothalamic neurons. J. Neurophysiol. 79: 716-726, 1998.
36. A receptor delta subunit with the alpha6 or alpha4 subunits? Soc. Neurosci Abstr. 24: 103, 1998.
37. A receptor stimulation promotes survival of embryonic rat striatal neurons in culture. Brain Res. Dev. Brain Res. 98: 253-258, 1997.
38. ISAAC, J.T.R., CRAIR, M. D., NICOLL, R. A., AND MALENKA, R. C. Silent synapses during development of thalamocortical inputs. Neuron 18: 269-280, 1997.
39. A receptor channel function in the nervous system. Prog. Neurobiol. 42: 489-537, 1994.
40. KANDLER, K. AND KATZ, L. C. Relationship between dye coupling and spontaneous activity in developing ferret visual cortex. Dev. Neurosci. 20: 59-64, 1998.
41. KIM, H. G., FOX, K., AND CONNORS, B. W. Properties of excitatory synaptic events in neurons of primary somatosensory cortex of neonatal rats. Cereb. Cortex. 5: 148-157, 1995.
42. KRIEGSTEIN, A. R., SUPPES, T., AND PRINCE, D. A. Cellular and synaptic physiology and epileptogenesis of developing rat neocortical neurons in vitro. Brain Res. 431: 161-171, 1987.
43. KRNJEVIC, K. AND SCHWARTZ, S. The action of gamma-aminobutyric acid on cortical neurones. Exp. Brain Res. 3: 320-336, 1967.
44. LAUDER, J. M., HAN, V. K., HENDERSON, P., VERDOORN, T., AND TOWLE, A. C. Prenatal ontogeny of the GABAergic system in the rat brain: an immunocytochemical study. Neuroscience 19: 465-493, 1986.
45. A receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J. Neurosci. 12: 4151-4172, 1992.
46. LOTURCO, J. J., BLANTON, M. G., AND KRIEGSTEIN, A. R. Initial expression and endogenous activation of NMDA channels in early neocortical development. J. Neurosci. 11: 792-799, 1991.
47. LOTURCO, J. J. AND KRIEGSTEIN, A. R. Clusters of coupled neuroblasts in embryonic neocortex. Science 252: 563-566, 1991.
48. LOTURCO, J. J., OWENS, D. F., HEATH, M.J.S., DAVIS, M.B.E., AND KRIEGSTEIN, A. R. GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15: 1287-1298, 1995.
49. LUHMANN, H. J. AND PRINCE, D. A. Postnatal maturation of the GABAergic system in rat neocortex. J. Neurophysiol. 65: 247-263, 1991.
50. A receptor alpha 4, beta 1, and gamma 1 subunits in the proliferative zone of the embryonic rat central nervous system. J. Neurosci. 15: 2547-2560, 1995.
51. A receptor channels. Annu. Rev. Neurosci. 17: 569-602, 1994.
52. MARTY, S., BERNINGER, B., CARROLL, P., AND THOENEN, H. GABAergic stimulation regulates the phenotype of hippocampal interneurons through the regulation of brain-derived neurotrophic factor. Neuron 16: 565-570, 1996.
53. MARTY, S., BERZAGHI MDA, P., AND BERNINGER, B. Neurotrophins and activity-dependent plasticity of cortical interneurons. Trends Neurosci. 20: 198-202, 1997.
54. A-receptor subtypes really occur in the brain? Trends Neurosci. 19: 139-143, 1996.
55. MEIER, E., HERTZ, L., AND SCHOUSBOE, A. Neurotransmitters as developmental signals. Neurochem. Int. 19: 1-15, 1991.
56. MICHEVA, K. D. AND BEAULIEU, C. Quantitative aspects of synaptogenesis in the rat barrel field cortex with special reference to GABA circuitry. J. Comp. Neurol. 373: 340-354, 1996.
57. MIENVILLE, J. M., LANGE, G. D., AND BARKER, J. L. Reciprocal expression of cell-cell coupling and voltage-dependent Na current during embryogenesis of rat telencephalon. Brain Res. Dev. Brain Res. 77: 89-95, 1994.
58. MODY, I., DE KONINCK, Y., OTIS, T. S., AND SOLTESZ, I. Bridging the cleft at GABA synapses in the brain. Trends Neurosci. 17: 517-525, 1994.
59. MORSE, D. E., DUNCAN, H., HOOKER, N., BALOUN, A., AND YOUNG, G. GABA induces behavioral and developmental metamorphosis in planktonic molluscan larvae. Fed. Proc. 39: 3237-3241, 1980.
60. Moss, S. J. AND SMART, T. G. Modulation of amino acid-gated ion channels by protein phosphorylation. Int Rev. Neurobiol. 39: 1-52, 1996.
61. A receptors in acutely dissociated P2-P6 rat hippocampal neurons. J. Neurophysiol. 79: 1321-1328, 1998.
62. NADARAJAH, B., JONES, A. M., EVANS, W. H., AND PARNAVELAS, J. G. Differential expression of connexins during neocortical development and neuronal circuit formation. J. Neurosci. 17: 3096-3111, 1997.
63. NEHER, E. Correction of liquid junction potentials in patch clamp experiments. Methods Enzymol. 207: 123-131, 1992.
64. OWENS, D. F., BOYCE, L. H., DAVIS, M.B.E., AND KRIEGSTEIN, A. R. Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated patch recordings and calcium imaging. J. Neurosci. 16: 6414-6423, 1996.
65. PEINADO, A., YUSTE, R., AND KATZ, L. C. Extensive dye coupling between rat neocortical neurons during the period of circuit formation. Neuron 10: 103-114, 1993.
66. A receptor alpha-subunit mRNAs in the developing rat CNS. J. Neurosci. 12: 2888-2900, 1992.
67. A receptor beta 2, beta 3 and gamma 2 subunit messenger RNAs during embryogenesis and early postnatal development of the rat central nervous system. Neuroscience 53: 1019-1033, 1993.
68. C receptors. Trends Neurosci. 19: 190, 1996.
69. RABOW, L. E., RUSSEK, S. J., AND FARB, D. H. From ion currents to genomic analysis: recent advances in GABAA receptor research. Synapse 21: 189-274, 1995.
70. REICHLLNG, D. B., KYROZIS, A., WANG, J., AND MACDERMOTT, A. B. Mechanisms of GABA and glycine depolarization-induced calcium transients in rat dorsal horn neurons. J. Physiol. (Lond.) 476.3: 411-421, 1994.
71. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397: 251-255, 1999.
72. A receptor-mediated responses in spinal neurons. J. Neurosci. 16: 82-91, 1996.
73. RORIG, B., KLAUSA, G., AND SUTOR, B. Intracellular acidification reduced gap junction coupling between immature rat neocortical pyramidal neurones. J. Physiol. (Lond.) 490: 31-49, 1996.
74. A receptor-mediated inhibitory currents in adult rat somatosensory cortex. J. Neurophysiol. 75: 1573-1588, 1996.
75. A receptor subunits: role of the delta subunit. J. Neurosci. 14: 7077-7086, 1994.
76. SAXENA, N. C. AND MACDONALD, R. L. Properties of putative cerebellar gamma-aminobutyric acid A receptor isoforms. Mol. Pharmacol. 49: 567-579, 1996.
77. - channels in embryonic rat spinal and olfactory bulb cells. J. Physiol. (Lond.) 488.2: 371-386, 1995.
78. SHIEH, P. B., HU, S. C., BOBB, K., TIMMUSK, T., AND GHOSH, A. Identification of a signaling pathway involved in calcium regulation of BDNF expression. Neuron 20: 727-740, 1998.
79. STRATA, F. AND CHERUBINI, E. Transient expression of a novel type of GABA response in rat CA3 hippocampal neurones during development. J. Physiol. (Lond.) 480: 493-503, 1994.
80. TAO, X., FINKBEINER, S., ARNOLD, D. B., SHAYWITZ, A. J., AND GREENBERG, M. E. Ca2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 20: 709-726, 1998.
81. TAYLOR, J., DOCHERTY, M., AND GORDON-WEEKS, P. R. GABAergic growth cones: release of endogenous gamma-aminobutyric acid precedes the expression of synaptic vesicle antigens. J. Neurochem. 54: 1689-1699, 1990.
82. TRAPIDO-ROSENTHAL, H. G. AND MORSE, D. E. Availability of chemosensory receptors is down-regulated by habituation of larvae to a morphogenetic signal. Proc. Natl. Acad. Sci. USA 83: 7658-7662, 1986.
83. - channels are randomly activated by continuous GABA secretion in cultured embryonic rat hippocampal neurons. Neurosci. Lett. 155: 199-203, 1993.
84. VAN EDEN, C. G., MRZLJAK, L., VOORN, P., AND UYLINGS, H. B. Prenatal development of GABA-ergic neurons in the neocortex of the rat. J. Comp. Neurol. 289: 213-227, 1989.
85. 2+ transients in embryonic rat dorsal horn neurons in culture. Eur. J. Neurosci. 6: 1275-1280, 1994.
86. A receptor subunit conferring atypical functional properties. J. Neurosci. 17: 5027-5037, 1997.
87. WU, W., ZISKIND-CONHAIM, L., AND SWEET, M. Early development of glycine and GABA-mediated synapses in rat spinal cord. J. Neurosci 12: 3935-3945, 1992.
88. A receptor-mediated currents in interneurons and pyramidal cells of rat visual cortex. J. Physiol. (Lond.) 506: 715-730, 1998.
89. YAMASHITA, M. AND FUKUDA, Y. Calcium channels and GABA receptors in the early embryonic chick retina. J. Neurobiol. 24: 1600-1614, 1993.
90. 2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron 6: 333-344, 1991.