Regulation of intracellular Cl- levels by Na+-dependent Cl- cotransport distinguishes depolarizing from hyperpolarizing GABAA receptor-mediated responses in spinal neurons

Journal of Neuroscience

Volumn 16, Issue 1, 1996, Pages 82-91

  Rohrbough, Jeffrey ^a   Spitzer, Nicholas C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Chloride; Chloride transport; Depolarization; Development; GABA; Spinal neurons

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID B RECEPTOR; CHLORIDE ION; SODIUM ION;

ANIMAL CELL; ARTICLE; CHLORIDE CONDUCTANCE; CHLORIDE TRANSPORT; DEPOLARIZATION; ELECTROPHYSIOLOGY; HYPERPOLARIZATION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; SODIUM TRANSPORT; SPINAL CORD NERVE CELL; XENOPUS LAEVIS;

ANIMALS; BIOLOGICAL TRANSPORT; CALCIUM CHANNELS; CARRIER PROTEINS; CHLORIDES; GAMMA-AMINOBUTYRIC ACID; LARVA; MEMBRANE POTENTIALS; NEURONS; PATCH-CLAMP TECHNIQUES; RECEPTORS, GABA-A; SODIUM; SODIUM CHLORIDE SYMPORTERS; SPINAL CORD; SYMPORTERS; XENOPUS LAEVIS;

EID: 0029670811     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-01-00082.1996     Document Type: Article

References (55)

1. Alvarez-Leefmans FJ, Gamin̄o SM, Giraldez F, Noguerón I (1988) Intracellular chloride regulation in amphibian dorsal root ganglion neurons studied with ion-selective microelectrodes. J Physiol (Lond) 406:225-246.
2. Andersen P, Dingledine R, Gjerstad L, Langmoen IA, Laursen AM (1980) Two different responses of hippocampal pyramidal cells to application of gamma-aminobutyric acid. J Physiol (Lond) 305:279-296.
3. Baccaglini PI, Spitzer NC (1977) Developmental changes in the inward current of the action potential of Rohon-Beard neurones. J Physiol (Lond) 271:93-117.
4. Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL (1989) Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol (Lond) 416:303-325.
5. Bixby JL, Spitzer NC (1982) The appearance and development of chemosensitivity in Rohon-Beard neurones of the Xenopus spinal cord. J Physiol (Lond) 330:513-536.
6. Bormann J, Hamili OP, Sakmann B (1987) Mechanism of anion permeation through channels gated by glycine and gamma-aminobutyric acid in mouse cultured spinal neurones. J Physiol (Lond) 385:243-286.
7. Cass A, Finkelstein A, Krespi V (1970) The ion permeability induced in thin lipid membranes by the polyene antibiotics nystatin and amphotericin B. J Gen Physiol 56:100-124.
8. Cherubini E, Gaiarsa JL, Ben-Ari Y (1991) GABA: an excitatory transmitter in early postnatal life. Trends Neurosci 14:515-519.
9. Cherubini E, Rovira C, Gaiarsa JL, Corradetti R, Ben-Ari Y (1990) GABA mediated excitation in immature rat CA3 hippocampal regions. Int J Dev Neurosci 8:481-490.
10. Clarke JDW, Roberts A (1984) Interneurones in the Xenopus embryo spinal cord: sensory excitation and activity during swimming. J Physiol (Lond) 354:345-362.
11. 2+ of rat cerebellar granule cells in explant cultures. J Neurosci 7:1384-1400.
12. Desarmenien MG, Spitzer NC (1991) Determinant role of calcium and protein kinase C in development of the delayed rectifier potassium current in Xenopus spinal neurons. Neuron 7:797-805.
13. Gallagher JP, Nakamura J, Shinnick-Gallagher P (1983) The effects of temperature, pH and Cl-pump inhibitors on GABA responses recorded from cat dorsal root ganglia. Brain Res 267:249-259.
14. A receptor-mediated responses in pyramidal cells of rat hippocampus. J Neurophysiol 69:1541-1554.
15. 2+ transients. Nature 375: 784-787.
16. Haas M (1989) Properties and diversity of (Na-K-Cl) cotransporters. Annu Rev Physiol 51:443-457.
17. - in rat hippocampal neurons. Neurosci Lett 143:135-138.
18. Hladky SB, Haydon DA (1984) Ion movements in gramicidin channels. Curr Top Membr Transp 21:327-372.
19. Holliday J, Spitzer NC (1990) Spontaneous calcium influx and its roles in differentiation of spinal neurons in culture. Dev Biol 141:13-23.
20. Horn R, Marty A (1988) Muscarinic activation of ionic currents measured by a new whole-cell recording method. J Gen Physiol 92:145-159.
21. Janigro D, Schwartzkroin PA (1988a) Effects of GABA on CA3 pyramidal cell dendrites in rabbit hippocampus. Brain Res 453:265-274.
22. Janigro D, Schwartzkroin PA (1988b) Effects of GABA and baclofen on pyramidal cells in the developing rabbit hippocampus. Brain Res 469:171-184.
23. A receptor-mediated IPSPs of rat neocortical neurons. J Physiol (Lond) 464:273-289.
24. Kleinberg ME, Finkelstein A (1984) Single-length and double-length channels formed by nystatin in lipid bilayer membranes. J Membr Biol 80:257-269.
25. Kyrozis A, Reichling DB (1995) Perforated-patch recording with gramicidin avoids artifactual changes in intracellular chloride concentration. J Neurosci Methods 57:27-35.
26. A receptor-mediated dendritic inhibition in area CA1 of the rat hippocampus. J Neurophysiol 66:1538-1548.
27. Luhmann HJ, Prince DA (1991) Postnatal maturation of the GABAergic system in rat neocortex. J Neurophysiol 65:247-263.
28. A receptor channels. Annu Rev Neurosci 17.569-602.
29. Mandler RN, Scahner AE, Novotny EA, Lange GD, Smith SV, Barker JL (1990) Electrical and chemical excitability appear one week before birth in the embryonic rat spinal cord. Brain Res 522:46-54.
30. Marty A, Finkelstein A (1975) Pores formed in lipid bilayer membrane by nystatin: differences in its one-sided and two-sided action. J Gen Physiol 65:515-526.
31. A receptors in the hippocampus. Science 253:1420-1423.
32. Misgeld U, Deisz RA, Dodt HU, Lux HD (1986) The role of chloride transport in postsynaptic inhibition of hippocampal neurons. Science 232:1413-1415.
33. Mueller AL, Taube JS, Schwartzkroin PA (1984) Development of hyperpolarizing inhibitory postsynaptic potentials and hyperpolarizing responses to γ-aminobutyric acid in rabbit hippocampus studied in vitro. J Neurosci 4:860-867.
34. Müller W, Misgeld U, Lux HD (1989) γ-Aminobutyric acid-induced ion movements in the guinea pig hippocampal slice. Brain Res 484: 184-191.
35. Neher E (1992) Correction for liquid junction potentials in patch clamp experiments. Methods Enzymol 207:123-131.
36. Nicoll RA (1978) The blockade of GABA mediated responses in the frog spinal cord by ammonium ions and furosemide. J Physiol (Lond) 283:121-132.
37. Nieuwkoop PD, Faber J (1965) Normal tables for Xenopus laevis, 2nd Ed (Daudin). Amsterdam: North-Holland.
38. Rae J, Cooper K, Gates G, Watsky M (1991) Low access resistance perforated patch recordings using aruphotericin B. J Neurosci Methods 37:15-26.
39. Reichling DB, Kyrozis A, Wang J, MacDermott AB (1994) Mechanisms of GABA and glycine depolarization-induced calcium transients in rat dorsal horn neurons. J Physiol (Lond) 476:411-421.
40. Rhee J-S, Ebihara S, Akaike N (1994) Gramicidin perforated patch-clamp technique reveals glycine-gated outward chloride current in dissociated nucleus solitarii neurons of rat. J Neurophysiol 72:1103-1108.
41. Roberts A, Clarke JDW (1982) The neuroanatomy of an amphibian embryo spinal cord. Philos Trans R Soc Lond [Biol] 296:195-212.
42. Roberts A, Dale N, Otterson OP, Storm-Mathisen J (1987) The early development of neurons with GABA immunoreactivity in the CNS of Xenopus laevis embryos. J Comp Neurol 261:435-449.
43. Robinson RA, Stokes RH (1965) Electrolyte solutions: the measurement and interpretation of conductance, chemical potential and diffusion in solutions of simple electrolytes, 2nd Ed. London: Butterworths.
44. A receptors. Soc Neurosci Abstr 20:1725.
45. Russell JM, Eaton DC, Brodwick MS (1977) Effects of nystatin on membrane conductance and internal ion activities in Aplysia neurons. J Membr Biol 37:137-156.
46. Sillar KT, Roberts A (1991) Segregation of NMDA and non-NMDA receptors at separate synaptic contacts: evidence from spontaneous EPSPs in Xenopus embryo spinal neurones. Brain Res 545:24-32.
47. Sillar KT, Simmers J (1994) Presynaptic inhibition of primary afferent transmitter release by 5-hydroxytryptamine at a mechanosensory synapse in the vertebrate spinal cord. J Neurosci 14:2636-2647.
48. Spitzer NC, deBaca RC, Allen KA, Holliday J (1993) Calcium dependence of differentiation of GABA immunoreactivily in spinal neurons. J Comp Neurol 337:168-175.
49. A receptors. Science 269:977-981.
50. Thompson SM, Deisz RA, Prince DA (1988) Relative contributions of passive equilibrium and active transport to the distribution of chloride in mammalian cortical neurons. J Neurophysiol 60:105-124.
51. 2+ transients in embryonic rat dorsal horn neurons in culture. J Neurosci 6:1275-1280.
52. Wojtowicz JM, Nicoll RA (1982) Selective action of piretanide on primary afferent GABA responses in the frog spinal cord. Brain Res 236:173-181.
53. Wu W-I, Ziskind-Conhaim L, Sweet MA (1992) Early development of glycine- and GABA-mediated synapses in rat spinal cord. J Neurosci 12:3935-3945.
54. 2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron 6:333-344.
55. Zhang L, Spigelman I, Carlen PL (1991) Development of GABA-mediated, chloride-dependent inhibition in CA1 pyramidal neurones of immature rat hippocampal slices. J Physiol (Lond) 444:25-49.