Shift of intracellular chloride concentration in ganglion and amacrine cells of developing mouse retina

Journal of Neurophysiology

Volumn 95, Issue 4, 2006, Pages 2404-2416

  Zhang, Ling Li ^a   Pathak, Hemal R ^a   Coulter, Douglas A ^a,b   Freed, Michael A ^a   Vardi, Noga ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; 6 METHOXY N ETHYLQUINOLINIUM IODIDE CHLORIDE; BICARBONATE; BUFFER; CALCIUM ION; CHLORIDE ION; FURA 2; GRAMICIDIN; IONOTROPIC RECEPTOR; QUINOLINE DERIVATIVE; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXTRACELLULAR CALCIUM; IMAGING SYSTEM; MOUSE; NERVE CELL; NERVE CELL STIMULATION; NERVE FIBER MEMBRANE STEADY POTENTIAL; NEWBORN; NONHUMAN; PERFORATION; PERINATAL PERIOD; PRIORITY JOURNAL; RETINA AMACRINE CELL; RETINA DEVELOPMENT;

ACTION POTENTIALS; AGING; AMACRINE CELLS; ANIMALS; ANIMALS, NEWBORN; CALCIUM; CALCIUM CHANNELS; CHLORIDES; DIAGNOSTIC IMAGING; FURA-2; GAMMA-AMINOBUTYRIC ACID; GRAMICIDIN; MEMBRANE POTENTIALS; MICE; MICROSCOPY, FLUORESCENCE; NEURAL INHIBITION; PATCH-CLAMP TECHNIQUES; QUINOLINIUM COMPOUNDS; RECEPTORS, GABA; RETINA; RETINAL GANGLION CELLS; TIME FACTORS;

EID: 33646200469     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00578.2005     Document Type: Article

References (67)

1. Bansal A, Singer JH, Hwang BJ, Xu W, Beaudet A, and Feller MB. Mice lacking specific nicotinic acetylcholine receptor subunits exhibit dramatically altered spontaneous activity patterns and reveal a limited role for retinal waves in forming ON and OFF circuits in the inner retina. J Neurosci 20: 7672-7681, 2000.
2. Becker DL, Bonness V, Catsicas M, and Mobbs P. Changing patterns of ganglion cell coupling and connexin expression during chick retinal development. J Neurobiol 52: 280-293, 2002.
3. Ben Ari Y. Developing networks play a similar melody. Trends Neurosci 24: 353-360, 2001.
4. Ben Ari Y. Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3: 728-739, 2002.
5. Bodnarenko SR and Chalupa LM. Stratification of ON and OFF ganglion cell dendrites depends on glutamate-mediated afferent activity in the developing retina. Nature 364: 144-146, 1993.
6. Bodnarenko SR, Jeyarasasingam G, and Chalupa LM. Development and regulation of dendritic stratification in retinal ganglion cells by glutamatemediated afferent activity. J Neurosci 15: 7037-7045, 1995.
7. Bormann J, Hamill OP, and Sakmann B. Mechanism of anion permeation through channels gated by glycine and gamma-aminobutryic acid in mouse cultured spinal neurons. J Physiol 385: 243-286, 1987.
8. B receptors regulate chick retinal calcium waves. J Neurosci 21: 897-910, 2001.
9. -] in P19-N cells reveals unique pharmacological properties. Brain Res 827: 1-11, 1999.
10. Diao L, Sun W, Deng Q, and He S. Development of the mouse retina: emerging morphological diversity of the ganglion cells. J Neurobiol 61: 236-249, 2004.
11. - regulation. J Physiol 520 Pt 1: 121-137, 1999.
12. 2+ signaling in developing rat cerebellar Purkinje neurones. J Physiol 536: 429-437, 2001.
13. Firth SI, Wang CT, and Feller MB. Retinal waves: mechanisms and function in visual system development. Cell Calcium 37: 425-432, 2005.
14. Fischer KF, Lukasiewicz PD, and Wong RO. Age-dependent and cell class-specific modulation of retinal ganglion cell bursting activity by GABA. J Neurosci 18: 3767-3778, 1998.
15. Fisher LJ. Development of synaptic arrays in the inner plexiform layer of neonatal mouse retina. J Comp Neurol 187: 359-372, 1979.
16. - in neurons in different layers of rat neocortical slices: advantages and limitations. Neurosci Res 32: 363-371, 1998.
17. Ganguly K, Schinder AF, Wong ST, and Poo M. GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 105: 521-532, 2001.
18. Guenther E, Rothe T, Taschenberger H, and Grantyn R. Separation of calcium currents in retinal ganglion cells from postnatal rat. Brain Res 633: 223-235, 1994.
19. Guenther E, Schmid S, Reiff D, and Zrenner E. Maturation of intrinsic membrane properties in rat retinal ganglion cells. Vision Res 39: 2477-2484, 1999.
20. Harms KJ, Tovar KR, and Craig AM. Synapse-specific regulation of AMPA receptor subunit composition by activity. J Neurosci 25: 6379-6388, 2005.
21. Hinkle PM, Shanshala ED, and Nelson EJ. Measurement of intracellular cadmium with fluorescent dyes. Further evidence for the role of calcium channels in cadmium uptake. J Biol Chem 267: 25553-25559, 1992.
22. 2+]i in retinal neurons of postnatal rabbits. Vis Neurosci 13: 441-447, 1996.
23. A and NMDA receptors in the suprachiasmatic nucleus. Eur J Neurosci 17: 58-70, 2003.
24. - and cell volume. J Neurochem 71: 1396-1404, 1998.
25. Inglefield JR and Schwartz-Bloom RD. Fluorescence imaging of changes in intracellular chloride in living brain slices. Methods 18: 197-203, 1999.
26. Kaila K, Pasternack M, Saarikoski J, and Voipio J. Influence of GABA-gated bicarbonate conductance on potential, current and intracellular chloride in crayfish muscle fibers. J Physiol 416: 161-181, 1989.
27. Kaneko H, Nakamura T, and Lindemann B. Noninvasive measurement of chloride concentration in rat olfactory receptor cells with use of a fluorescent dye. Am J Physiol Cell Physiol 280: C1387-C1393, 2001.
28. Kaneko H, Putzier I, Frings S, Kaupp UB, and Gensch T. Chloride accumulation in mammalian olfactory sensory neurons. J Neurosci 24: 7931-7938, 2004.
29. A receptors, and synapse-associated proteins in the developing and adult ferret retina. Vis Neurosci 14: 1097-1108, 1997.
30. Katz LC and Shatz CJ. Synaptic activity and the construction of cortical circuits. Science 274: 1133-1138, 1996.
31. Koizumi A, Jakobs TC, and Masland RH. Inward rectifying currents stabilize the membrane potential in dendrites of mouse amacrine cells: patch-clamp recordings and single-cell RT-PCR. Mol Vis 10: 328-340, 2004.
32. Krapf R, Berry CA, and Verkman AS. Estimation of intracellular chloride activity in isolated perfused rabbit proximal convoluted tubules using a fluorescent indicator. Biophys J 53: 955-962, 1988.
33. 2+ rise in pyramidal cells and interneurons from rat neonatal hippocampal slices. J Physiol 487: 319-329, 1995.
34. Lichtman JW and Colman H. Synapse elimination and indelible memory. Neuron 25: 269-278, 2000.
35. A receptors mediate trophic effects of GABA on embryonic brainstem monoamine neurons in vitro. J Neurosci 17: 2420-2428, 1997.
36. Marandi N, Konnerth A, and Garaschuk O. Two-photon chloride imaging in neurons of brain slices. Pfluegers 445: 357-365, 2002.
37. 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.
38. Miller RF and Dacheux RF. Intracellular chloride in retinal neurons: measurement and meaning. Vision Res 23: 399-411, 1983.
39. Nakamura T, Kaneko H, and Nishida N. Direct measurement of the chloride concentration in newt olfactory receptors with the fluorescent probe. Neurosci Lett 237: 5-8, 1997.
40. Olney JW. Centripetal sequence of appearance of receptor-bipolar synaptic structures in developing mouse retina. Nature 218: 281-282, 1968.
41. Owens DF, Boyce LH, Davis MB, and Kriegstein AR. Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J Neurosci 16: 6414-6423, 1996.
42. Penn AA, Riquelme PA, Feller MB, and Shatz CJ. Competition in retinogeniculatepatterning driven by spontaneous activity. Science 279: 2108-2112, 1998.
43. Penn AA, Wong RO, and Shatz CJ. Neuronal coupling in the developing mammalian retina. J Neurosci 14: 3805-3815, 1994.
44. Redburn DA. Development of GABAergic neurons in the mammalian retina. Prog Brain Res 90: 133-147, 1992.
45. Rothe T, Juttner R, Bahring R, and Grantyn R. Ion conductances related to development of repetitive firing in mouse retinal ganglion neurons in situ. J Neurobiol 38: 191-206, 1999.
46. A receptors, and the anchoring protein gephyrin. J Comp Neurol 381: 158-174, 1997.
47. 2+ currents in rat retinal ganglion cells. Neuroreport 7: 677-681, 1996.
48. Sernagor E, Young C, and Eglen SJ. Developmental modulation of retinal wave dynamics: shedding light on the GABA saga. J Neurosci 23: 7621-7629, 2003.
49. Shatz CJ and Stryker MP. Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. Science 242: 87-89, 1988.
50. Sherry DM, Wang MM, Bates J, and Frishman LJ. Expression of vesicular glutamate transporter 1 in the mouse retina reveals temporal ordering in development of rod vs. cone and ON vs. OFF circuits. J Comp Neurol 465: 480-498, 2003.
51. Stacy RC and Wong RO. Developmental relationship between cholinergic amacrine cell processes and ganglion cell dendrites of the mouse retina. J Comp Neurol 456: 154-166, 2003.
52. Syed MM, Lee S, Zheng J, and Zhou ZJ. Stage-dependent dynamics and modulation of spontaneous waves in the developing rabbit retina. J Physiol 560: 533-549, 2004.
53. Thoreson WB and Bryson EJ. Chloride equilibrium potential in salamander cones. BMC Neurosci 5:53, 2004.
54. Thoreson WB, Nitzan R, and Miller RF. Chloride efflux inhibits single calcium channel open probability in vertebrate photoreceptors: chloride imaging and cell-attached patch-clamp recordings. Vis Neurosci 17: 197-206, 2000.
55. Ueda Y, Iwakabe H, Masu M, Suzuki M, and Nakanishi S. The mGluR6 5′ upstream transgene sequence directs a cell-specific and developmentally regulated expression in retinal rod and ON-type cone bipolar cells. J Neurosci 17: 3014-3023, 1997.
56. Verkman AS. Development and biological applications of chloride-sensitivefluorescent indicators. Am J Physiol Cell Physiol 259: C375-C388, 1990.
57. Vu TQ, Payne JA, and Copenhagen DR. Localization and developmental expression patterns of the neuronal K-Cl cotransporter (KCC2) in the rat retina. J Neurosci 20: 1414-1423, 2000.
58. + conductances on spontaneous discharge patterns of developing retinal ganglion cells. J Neurosci 19: 2609-2618, 1999.
59. Watanabe S, Koizumi A, Matsunaga S, Stocker JW, and Kaneko A. GABA-mediated inhibition between amacrine cells in the goldfish retina. J Neurophysiol 84: 1826-1834, 2000.
60. Wiesel TN. Postnatal development of the visual cortex and the influence of environment. Nature 299: 583-591, 1982.
61. Wong WT and Wong RO. Changing specificity of neurotransmitter regulation of rapid dendritic remodeling during synaptogenesis. Nat Neurosci 4: 351-352, 2001.
62. - uptake promoting depolarizing GABA actions in immature rat neocortical neurons is mediated by NKCC1. J Physiol 557: 829-841, 2004.
63. Young TL and Cepko CL. A role for ligand-gated ion channels in rod photoreceptor development. Neuron 41: 867-879, 2004.
64. 2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron 6: 333-344, 1991.
65. Zheng JJ, Lee S, and Zhou ZJ. A developmental switch in the excitability and function of the starburst network in the mammalian retina. Neuron 44: 851-864, 2004.
66. Zhou ZJ. Direct participation of starburst amacrine cells in spontaneous rhythmic activities in the developing mammalian retina. J Neurosci 18: 4155-4165, 1998.
67. Zhou ZJ. A critical role of the strychnine-sensitive glycinergic system in spontaneous retinal waves of the developing rabbit. J Neurosci 21: 5158-5168, 2001.