The GABAergic system in the retina of neonate and adult Octodon degus, studied by immunohistochemistry and electroretinography

Journal of Comparative Neurology

Volumn 514, Issue 5, 2009, Pages 459-472

  Delgado, Luz M ^a   Vielma, Alex H ^a   Kähne, Thilo ^b   Palacios, Adrián G ^a   Schmachtenberg, Oliver ^a  

^a UNIVERSIDAD DE VALPARAÍSO   (Chile)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

Development; Electroretinogram; GABA; Octodon degus; Retina; Vision

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID C RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; BICUCULLINE; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; (1,2,5,6 TETRAHYDROPYRIDIN 4 YL)METHYLPHOSPHINIC ACID; (1,2,5,6-TETRAHYDROPYRIDIN-4-YL)METHYLPHOSPHINIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 1; GLUTAMATE DECARBOXYLASE 2; PHOSPHINIC ACID DERIVATIVE; PYRIDINE DERIVATIVE;

AGE DISTRIBUTION; AMINO ACID SYNTHESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ELECTRORETINOGRAPHY; EYE MOVEMENT; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; IMMUNOHISTOCHEMISTRY; NEWBORN; NONHUMAN; OCTODON; OCTODON DEGUS; PERINATAL PERIOD; PHOTOREACTIVITY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RETINA AMACRINE CELL; RETINA CONE; RETINA DEVELOPMENT; RETINA GANGLION CELL; RETINA INNER PLEXIFORM LAYER; RETINA ROD; SIGNAL TRANSDUCTION; ULTRAVIOLET RADIATION; ANIMAL; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PERCEPTIVE THRESHOLD; PHOTOSTIMULATION; RETINA; VISION; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; BICUCULLINE; BLOTTING, WESTERN; ELECTRORETINOGRAPHY; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; IMMUNOHISTOCHEMISTRY; OCTODON; PHOSPHINIC ACIDS; PHOTIC STIMULATION; PYRIDINES; RECEPTORS, GABA; RETINA; SENSORY THRESHOLDS; SIGNAL TRANSDUCTION; ULTRAVIOLET RAYS; VISION, OCULAR;

EID: 66149111452     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22023     Document Type: Article

References (111)

1. Agardh E, Bruun A, Ehinger B, Storm-Mathisen J. 1986. GABA immunoreactivity in the retina. Invest Ophthalmol Vis Sci 27:674-678.
2. Bahring R, Standhardt H, Martelli EA, Grantyn R. 1994. GABA-activated chloride currents of postnatal mouse retinal ganglion cells are blocked by acetylcholine and acetylcarnitine: how specific are ion channels in immature neurons? Eur J Neurosci 6:1089-1099.
3. Belhage B, Hansen GH, Elster L, Schousboe A. 1998. Effects of gamma-aminobutyric acid (GABA) on synaptogenesis and synaptic function. Perspect Dev Neurobiol 5:235-246.
4. Ben-Ari Y. 2002. Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 3:728-739.
5. Bowery NG, Bettler B, Froestl W, Gallagher JP, Marshall F, Raiteri M, Bonner TI, Enna SJ. 2002. International Union of Pharmacology. XXXIII. Mammalian gamma-aminobutyric acid(B) receptors: structure and function. Pharmacol Rev 54:247-264.
6. Boycott B, Wässle H. 1999. Parallel processing in the mammalian retina: the Proctor Lecture. Invest Ophthalmol Vis Sci 40:1313-1327.
7. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
8. Brandstatter JH, Greferath U, Euler T, Wässle H. 1995. Co-stratification of GABAA receptors with the directionally selective circuitry of the rat retina. Vis Neurosci 12:345-358.
9. Breton ME, Quinn GE, Schueller AW. 1995. Development of electroretinogram and rod phototransduction response in human infants. Invest Ophthalmol Vis Sci 36:1588-1602.
10. Bui BV, Vingrys AJ. 1999. Development of receptoral responses in pigmented and albino guinea-pigs (Cavia porcellus). Doc Ophthalmol 99:151-170.
11. Chavez AE, Bozinovic F, Peichl L, Palacios AG. 2003. Retinal spectral sensitivity, fur coloration, and urine reflectance in the genus Octodon (Rodentia): implications for visual ecology. Invest Ophthalmol Vis Sci 44:2290-2296.
12. Chebib M. 2004. GABAC receptor ion channels. Clin Exp Pharmacol Physiol 31:800-804.
13. Chun MH, Wässle H. 1989. GABA-like immunoreactivity in the cat retina: electron microscopy. J Comp Neurol 279:55-67.
14. Curtis DR, Duggan AW, Felix D, Johnston GA. 1970. GABA, bicuculline and central inhibition. Nature 226:1222-1224.
15. Dkhissi O, Julien JF, Wasowicz M, Dalil-Thiney N, Nguyen-Legros J, Versaux-Botteri C. 2001. Differential expression of GAD(65) and GAD(67) during the development of the rat retina. Brain Res 919:242-249.
16. Dong CJ, Hare WA. 2002. GABAc feedback pathway modulates the amplitude and kinetics of ERG b-wave in a mammalian retina in vivo. Vision Res 42:1081-1087.
17. Du JL, Yang XL. 2000. Subcellular localization and complements of GABA(A) and GABA(C) receptors on bullfrog retinal bipolar cells. J Neurophysiol 84:666-676.
18. el-Azazi M, Wachtmeister L. 1990. The postnatal development of the oscillatory potentials of the electroretinogram. I. Basic characteristics. Acta Ophthalmol (Copenh) 68:401-409.
19. Eliasson MJ, McCaffery P, Baughman RW, Drager UC. 1997. A ventrodorsal GABA gradient in the embryonic retina prior to expression of glutamate decarboxylase. Neuroscience 79:863-869.
20. Engbretson GA, Anderson KJ, Wu JY. 1988. GABA as a potential transmitter in lizard photoreceptors: immunocytochemical and biochemical evidence. J Comp Neurol 278:461-471.
21. Enz R, Brandstatter JH, Hartveit E, Wässle H, Bormann J. 1995. Expression of GABA receptor rho 1 and rho 2 subunits in the retina and brain of the rat. Eur J Neurosci 7:1495-1501.
22. Enz R, Brandstatter JH, Wässle H, Bormann J. 1996. Immunocytochemical localization of the GABAc receptor rho subunits in the mammalian retina. J Neurosci 16:4479-4490.
23. Erlander MG, Tobin AJ. 1991. The structural and functional heterogeneity of glutamic acid decarboxylase: a review. Neurochem Res 16:215-226.
24. Euler T, Masland RH. 2000. Light-evoked responses of bipolar cells in a mammalian retina. J Neurophysiol 83:1817-1829.
25. Euler T, Wässle H. 1998. Different contributions of GABAA and GABAC receptors to rod and cone bipolar cells in a rat retinal slice preparation. J Neurophysiol 79:1384-1395.
26. Feigenspan A, Bormann J. 1998. GABA-gated Cl-channels in the rat retina. Prog Retin Eye Res 17:99-126.
27. Fischer KF, Lukasiewicz PD, Wong RO. 1998. Age-dependent and cell class-specific modulation of retinal ganglion cell bursting activity by GABA. J Neurosci 18:3767-3778.
28. Fiszman ML, Behar T, Lange GD, Smith SV, Novotny EA, Barker JL. 1993. GABAergic cells and signals appear together in the early post-mitotic period of telencephalic and striatal development. Brain Res Dev Brain Res 73:243-251.
29. Fletcher EL, Kalloniatis M. 1997. Localization of amino acid neurotransmitters during postnatal development of the rat retina. J Comp Neurol 380:449-471.
30. Fletcher EL, Koulen P, Wässle H. 1998. GABAA and GABAC receptors on mammalian rod bipolar cells. J Comp Neurol 396:351-365.
31. Fong AY, Stornetta RL, Foley CM, Potts JT. 2005. Immunohistochemical localization of GAD67-expressing neurons and processes in the rat brainstem: subregional distribution in the nucleus tractus solitarius. J Comp Neurol 493:274-290.
32. Friedman DL, Redburn DA. 1990. Evidence for functionally distinct subclasses of gamma-aminobutyric acid receptors in rabbit retina. J Neurochem 55:1189-1199.
33. Gorfinkel J, Lachapelle P. 1990. Maturation of the photopic b-wave and oscillatory potentials of the electroretinogram in the neonatal rabbit. Can J Ophthalmol 25:138-144.
34. Gorfinkel J, Lachapelle P, Molotchnikoff S. 1988. Maturation of the electroretinogram of the neonatal rabbit. Doc Ophthalmol 69:237-245.
35. A receptor subunits have differential distributions in the rat retina: in situ hybridization and immunohistochemistry. J Comp Neurol 353:553-571.
36. Greka A, Lipton SA, Zhang D. 2000. Expression of GABA(C) receptor rho1 and rho2 subunits during development of the mouse retina. Eur J Neurosci 12:3575-3582.
37. Grunert U, Hughes TE. 1993. Immunohistochemical localization of GABAA receptors in the scotopic pathway of the cat retina. Cell Tissue Res 274:267-277.
38. Gum GG, Gelatt KN, Samuelson DA. 1984. Maturation of the retina of the canine neonate as determined by electroretinography and histology. Am J Vet Res 45:1166-1171.
39. Gurevich L, Slaughter MM. 1993. Comparison of the waveforms of the ON bipolar neuron and the b-wave of the electroretinogram. Vision Res 33:2431-2435.
40. Hamano K, Kiyama H, Emson PC, Manabe R, Nakauchi M, Tohyama M. 1990. Localization of two calcium binding proteins, calbindin (28 kD) and parvalbumin (12 kD), in the vertebrate retina. J Comp Neurol 302:417-424.
41. Hamasaki DI, Maguire GW. 1985. Physiological development of the kitten's retina: an ERG study. Vision Res 25:1537-1543.
42. Hu M, Bruun A, Ehinger B. 1998. The expression of GABA(A) receptors during the development of the rabbit retina. Acta Ophthalmol Scand 76:515-520.
43. Haverkamp S, Wässle H. 2000. Immunocytochemical analysis of the mouse retina. J Comp Neurol 424:1-23.
44. Huang BO, Redburn DA. 1996. GABA-induced increases in [Ca2+]i in retinal neurons of postnatal rabbits. Vis Neurosci 13:441-447.
45. Hughes TE, Carey RG, Vitorica J, de Blas AL, Karten HJ. 1989. Immunohistochemical localization of GABAA receptors in the retina of the New World primate Saimiri sciureus. Vis Neurosci 2:565-581.
46. Hughes TE, Grunert U, Karten HJ. 1991. GABAA receptors in the retina of the cat: an immunohistochemical study of wholemounts, sections, and dissociated cells. Vis Neurosci 6:229-238.
47. Ikeda H, Hankins MW, Kay CD. 1990. Actions of baclofen and phaclofen upon ON-and OFF-ganglion cells in the cat retina. Eur J Pharmacol 190:1-9.
48. Jacobs GH, Calderone JB, Fenwick JA, Krogh K, Williams GA. 2003. Visual adaptations in a diurnal rodent, Octodon degus. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 189:347-361.
49. Jacobson SG, Ikeda H, Ruddock K. 1987. Cone-mediated retinal function in cats during development. Doc Ophthalmol 65:7-14.
50. Kapousta-Bruneau NV. 2000. Opposite effects of GABA(A) and GABA(C) receptor antagonists on the b-wave of ERG recorded from the isolated rat retina. Vision Res 40:1653-1665.
51. Karne A, Oakley DM, Wong GK, Wong RO. 1997. Immunocytochemical localization of GABA, GABAA receptors, and synapse-associated proteins in the developing and adult ferret retina. Vis Neurosci 14:1097-1108.
52. Kirk GR, Boyer SF. 1973. Maturation of the electroretinogram in the dog. Exp Neurol 38:252-264.
53. Koulen P. 1999. Postnatal development of GABAA receptor beta1, beta2/3, and gamma2 immunoreactivity in the rat retina. J Neurosci Res 57:185-194.
54. Koulen P, Sassoe-Pognetto M, Grunert U, Wässle H. 1996. Selective clustering of GABA(A) and glycine receptors in the mammalian retina. J Neurosci 16:2127-2140.
55. Koulen P, Brandstatter JH, Kroger S, Enz R, Bormann J, Wässle H. 1997. Immunocytochemical localization of the GABA(C) receptor rho subunits in the cat, goldfish, and chicken retina. J Comp Neurol 380:520-532.
56. Koulen P, Brandstatter JH, Enz R, Bormann J, Wässle H. 1998a. Synaptic clustering of GABA(C) receptor rho-subunits in the rat retina. Eur J Neurosci 10:115-127.
57. Koulen P, Malitschek B, Kuhn R, Bettler B, Wässle H, Brandstatter JH. 1998b. Presynaptic and postsynaptic localization of GABA(B) receptors in neurons of the rat retina. Eur J Neurosci 10:1446-1456.
58. Kupenova P, Popova E, Vitanova L. 2008. GABAa and GABAc receptor mediated influences on the intensity-response functions of the b- and d-wave in the frog ERG. Vision Res 48:882-892.
59. Lauder JM, Han VK, Henderson P, Verdoorn T, Towle AC. 1986. Prenatal ontogeny of the GABAergic system in the rat brain: an immunocytochemical study. Neuroscience 19:465-493.
60. Loeliger M, Rees S. 2005. Immunocytochemical development of the guinea pig retina. Exp Eye Res 80:9-21.
61. Lukasiewicz PD, Maple BR, Werblin FS. 1994. A novel GABA receptor on bipolar cell terminals in the tiger salamander retina. J Neurosci 14(3 Pt 1):1202-1212.
62. Lukasiewicz PD, Eggers ED, Sagdullaev BT, McCall MA. 2004. GABAC receptor-mediated inhibition in the retina. Vision Res 44:3289-3296.
63. Marty A, Llano I. 2005. Excitatory effects of GABA in established brain networks. Trends Neurosci 28:284-289.
64. McCall MA, Lukasiewicz PD, Gregg RG, Peachey NS. 2002. Elimination of the rho1 subunit abolishes GABA(C) receptor expression and alters visual processing in the mouse retina. J Neurosci 22:4163-4174.
65. Messersmith EK, Redburn DA. 1992. gamma-Aminobutyric acid immunoreactivity in multiple cell types of the developing rabbit retina. Vis Neurosci 8:201-211.
66. Messersmith EK, Redburn DA. 1993. The role of GABA during development of the outer retina in the rabbit. Neurochem Res 18:463-470.
67. Mitchell CK, Redburn DA. 1996. GABA and GABA-A receptors are maximally expressed in association with cone synaptogenesis in neonatal rabbit retina. Brain Res Dev Brain Res 95:63-71.
68. Mitchell CK, Huang B, Redburn-Johnson DA. 1999. GABA(A) receptor immunoreactivity is transiently expressed in the developing outer retina. Vis Neurosci 16:1083-1088.
69. Mohler H. 2006. GABA(A) receptor diversity and pharmacology. Cell Tissue Res 326:505-516.
70. Mohler H, Benke D, Fritschy JM. 2001. GABA(B)-receptor isoforms molecular architecture and distribution. Life Sci 68:2297-2300.
71. Möller A, Eysteinsson T. 2003. Modulation of the components of the rat dark-adapted electroretinogram by the three subtypes of GABA receptors. Vis Neurosci 20:535-542.
72. Muller F, Boos R, Wässle H. 1992. Actions of GABAergic ligands on brisk ganglion cells in the cat retina. Vis Neurosci 9:415-425.
73. Naka KI, Rushton WA. 1966. S-potentials from colour units in the retina of fish (Cyprinidae). J Physiol 185:536-555.
74. Namchuk M, Lindsay L, Turck CW, Kanaani J, Baekkeskov S. 1997. Phosphorylation of serine residues 3, 6, 10, and 13 distinguishes membrane anchored from soluble glutamic acid decarboxylase 65 and is restricted to glutamic acid decarboxylase 65alpha. J Biol Chem 272:1548-1557.
75. Nishimura Y, Schwartz ML, Rakic P. 1986. GABA and GAD immunoreactivity of photoreceptor terminals in primate retina. Nature 320:753-756.
76. Osborne NN, Beaton DW. 1986. The occurrence of gamma-aminobutyric acid (GABA)-containing cells in cultures of retinas from the human fetus. Cell Mol Neurobiol 6:87-93.
77. Palma F, Vélez P, Kirkwood A, Palacios A. 2002. Contribution of GABA and glycine inhibitory receptors in the retina of the diurnal rodent, Octodon degu. Society for Neuroscience Meeting, November 2-7, Orlando, FL.
78. Peichl L, Gonzalez-Soriano J. 1994. Morphological types of horizontal cell in rodent retinae: a comparison of rat, mouse, gerbil, and guinea pig. Vis Neurosci 11:501-517.
79. Peichl L, Chavez AE, Ocampo A, Mena W, Bozinovic F, Palacios AG. 2005. Eye and vision in the subterranean rodent cururo (Spalacopus cyanus, Octodontidae). J Comp Neurol 486:197-208.
80. Pourcho RG, Owczarzak MT. 1989. Distribution of GABA immunoreactivity in the cat retina: a light-and electron-microscopic study. Vis Neurosci 2:425-435.
81. Racine J, Behn D, Lachapelle P. 2008. Structural and functional maturation of the retina of the albino Hartley guinea pig. Doc Ophthalmol 117:13-26.
82. Ragozzino D, Woodward RM, Murata Y, Eusebi F, Overman LE, Miledi R. 1996. Design and in vitro pharmacology of a selective gamma-aminobutyric acidC receptor antagonist. Mol Pharmacol 50:1024-1030.
83. Redburn DA, Madtes P Jr. 1986. Postnatal development of 3H-GABA-accumulating cells in rabbit retina. J Comp Neurol 243:41-57.
84. Redburn DA, Rowe-Rendleman C. 1996. Developmental neurotransmitters. Signals for shaping neuronal circuitry. Invest Ophthalmol Vis Sci 37:1479-1482.
85. Redburn-Johnson D. 1998. GABA as a developmental neurotransmitter in the outer plexiform layer of the vertebrate retina. Perspect Dev Neurobiol 5:261-267.
86. Reuter JH. 1976. The development of the electroretinogram in normal and light-deprived rabbits. Pflugers Arch 363:7-13.
87. Rohrenbeck J, Wässle H, Heizmann CW. 1987. Immunocytochemical labelling of horizontal cells in mammalian retina using antibodies against calcium-binding proteins. Neurosci Lett 77:255-260.
88. Rotolo TC, Dacheux RF. 2003. Evidence for glycine, GABAA, and GABAB receptors on rabbit OFF-alpha ganglion cells. Vis Neurosci 20:285-296.
89. Rowe-Rendleman C, Mitchell CK, Habrecht M, Redburn DA. 1996. Expression and downregulation of the GABAergic phenotype in explants of cultured rabbit retina. Invest Ophthalmol Vis Sci 37:1074-1083.
90. Rozzo A, Armellin M, Franzot J, Chiaruttini C, Nistri A, Tongiorgi E. 2002. Expression and dendritic mRNA localization of GABAC receptor rho1 and rho2 subunits in developing rat brain and spinal cord. Eur J Neurosci 15:1747-1758.
91. Sandell JH. 1998. GABA as a developmental signal in the inner retina and optic nerve. Perspect Dev Neurobiol 5:269-278.
92. Sassoe-Pognetto M, Wässle H. 1997. Synaptogenesis in the rat retina: subcellular localization of glycine receptors, GABA(A) receptors, and the anchoring protein gephyrin. J Comp Neurol 381:158-174.
93. Schnitzer J, Rusoff AC. 1984. Horizontal cells of the mouse retina contain glutamic acid decarboxylase-like immunoreactivity during early developmental stages. J Neurosci 4:2948-2955.
94. Shields CR, Tran MN, Wong RO, Lukasiewicz PD. 2000. Distinct ionotropic GABA receptors mediate presynaptic and postsynaptic inhibition in retinal bipolar cells. J Neurosci 20:2673-2682.
95. Slaughter MM, Pan ZH. 1992. The physiology of GABAB receptors in the vertebrate retina. Prog Brain Res 90:47-60.
96. Soghomonian JJ, Martin DL. 1998. Two isoforms of glutamate decarboxylase: why? Trends Pharmacol Sci 19:500-505.
97. Spira AW. 1975. In utero development and maturation of the retina of a non-primate mammal: a light and electron microscopic study of the guinea pig. Anat Embryol (Berl) 146:279-300.
98. Spoerri PE. 1988. Neurotrophic effects of GABA in cultures of embryonic chick brain and retina. Synapse 2:11-22.
99. Thoreson WB, Witkovsky P. 1999. Glutamate receptors and circuits in the vertebrate retina. Prog Retin Eye Res 18:765-810.
100. Vardi N, Auerbach P. 1995. Specific cell types in cat retina express different forms of glutamic acid decarboxylase. J Comp Neurol 351:374-384.
101. Varju P, Katarova Z, Madarasz E, Szabo G. 2001. GABA signaling during development: new data and old questions. Cell Tissue Res 305:239-246.
102. Wang CT, Blankenship AG, Anishchenko A, Elstrott J, Fikhman M, Nakanishi S, Feller MB. 2007. GABA(A) receptor-mediated signaling alters the structure of spontaneous activity in the developing retina. J Neurosci 27:9130-9140.
103. Weidman TA, Kuwabara T. 1969. Development of the rat retina. Invest Ophthalmol 8:60-69.
104. Woods JR Jr, Parisi V, Coppes V, Brooks DE. 1983. Maturational sequence of the visual system: serial measurements of visual evoked potential and electroretinogram in the healthy neonatal lamb. Am J Obstet Gynecol 145:738-743.
105. Xu H, Tian N. 2004. Pathway-specific maturation, visual deprivation, and development of retinal pathway. Neuroscientist 10:337-346.
106. Yamasaki EN, Barbosa VD, De Mello FG, Hokoc JN. 1999. GABAergic system in the developing mammalian retina: dual sources of GABA at early stages of postnatal development. Int J Dev Neurosci 17:201-213.
107. Yan XX. 1997. Prenatal development of calbindin D-28K and parvalbumin immunoreactivities in the human retina. J Comp Neurol 377:565-576.
108. Yang XL. 2004. Characterization of receptors for glutamate and GABA in retinal neurons. Prog Neurobiol 73:127-150.
109. Yeh HH, Lee MB, Cheun JE. 1990. Properties of GABA-activated whole-cell currents in bipolar cells of the rat retina. Vis Neurosci 4:349-357.
110. Zhang LL, Pathak HR, Coulter DA, Freed MA, Vardi N. 2006. Shift of intracellular chloride concentration in ganglion and amacrine cells of developing mouse retina. J Neurophysiol 95:2404-2416.
111. Zucker CL, Nilson JE, Ehinger B, Grzywacz NM. 2005. Compartmental localization of gamma-aminobutyric acid type B receptors in the cholinergic circuitry of the rabbit retina. J Comp Neurol 493:448-459.