Abstract
The expression of GABAC receptors has long been regarded as a specific property of bipolar cells in the inner retina where they control the information transfer from bipolar to retinal ganglion cells. A number of recent anatomical and physiological studies, however, have provided evidence that GABAC receptors are also expressed in many brain structures apart from the retina. The presence of GABAC receptors in many GABAergic neurons suggests that this receptor type may be involved in the regulation of local inhibition. This chapter focuses on the distribution of GABAC receptors and their possible function in various brain areas.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsPreview
Unable to display preview. Download preview PDF.
References
Alakuijala A, Palgi M, Wegelius K, Schmidt M, Enz R, Paulin L, Saarma M, Pasternack M (2005) GABA receptor ρ subunit expression in the developing rat brain. Dev Brain Res 154:15–23
Arakawa T, Okada Y (1988) Excitatory and inhibitory action of GABA on synaptic transmission in slices of guinea pig superior colliculus. Eur J Pharmacol 158:217–224
Ashmore JF, Copenhagen DR (1980) Different postsynaptic events in two types of retinal bipolar cell. Nature 288:84–86
Boller M, Schmidt M (2001) Postnatal maturation of GABAA and GABAC receptor function in the mammalian superior colliculus. Eur J Neurosci 14:1185–1193
Boller M, Schmidt M (2003) GABAC receptors in the rat superior colliculus and pretectum participate in synaptic neurotransmission. J Neurophysiol 89:2035–2045
Bormann J, Feigenspan A (1995) GABAC receptors. Trends Neurosci 18:515–519
Boué-Grabot E, Roudbaraki M, Bascles L, Tramu G, Bloch B, Garret M (1998) Expression of GABA receptor ρ subunits in rat brain. J Neurochem 70:899–907
Clark SE, Garret M, Platt B (2001) Postnatal alterations of GABA receptor profiles in the rat superior colliculus. Neuroscience 104:441–454
Cutting GR, Lu L, O'Hara BF, Kasch LM, Montrose-Rafizadeh C, Donovan DM, Shimada S, Antonarakis SE, Guggino WB, Uhl GR (1991) Cloning of the γ-aminobutyric acid (GABA) ρ1 cDNA: a GABA receptor subunit highly expressed in the retina. Proc Natl Acad Sci USA 88:2673–2677
Delaney AJ, Sah P (1999) GABA receptors inhibited by benzodiazepines mediate fast inhibitory transmission in the central amygdala. J Neurosci 19:9698–9704
DeVries SH, Schwartz EA (1999) Kainate receptors mediate synaptic transmission between cones and ‘Off’ bipolar cells in a mammalian retina. Nature 397:157–160
Didelon F, Sciancalepore M, Savic N, Mladinic M, Bradbury A, Cherubini E (2002) γ-Aminobutyric acidA ρ receptor subunits in the developing rat hippocampus. J Neurosci Res 67:739–744
Dong CJ, Picaud SA, Werblin FS (1994) GABA transporters and GABAC-like receptors on catfish cone- but not rod-driven horizontal cells. J Neurosci 14:2648–2658
Dong CJ, Werblin FS (1998) Temporal contrast enhancement via GABAC feedback at bipolar terminals in the tiger salamander retina. J Neurophysiol 79:2171–2180
Du JL, Yang XL (2000) Subcellular localization and complements of GABAA and GABAC receptors on bullfrog retinal bipolar cells. J Neurophysiol 84:666–667
Enz R, Brandstätter JH, Hartveit E, Wässle H, Bormann J (1995) Expression of GABA receptor ρ1 and ρ2 subunits in the retina and brain of the rat. Eur J Neurosci 7:1495–1501
Enz R, Brandstätter JH, Wässle H, Bormann J (1996) Immunocytochemical localization of the GABAC receptor ρ subunits in the mammalian retina. J Neurosci 16:4479–4490
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
Euler T, Masland RH (2000) Light-evoked responses of bipolar cells in a mammalian retina. J Neurophysiol 83:1817–1829
Feigenspan A, Wässle H, Bormann J (1993) Pharmacology of GABA receptor Cl-channels in rat retinal bipolar cells. Nature 361:159–162
Fletcher EL, Koulen P, Wässle H (1998) GABAA and GABAC receptors on mammalian rod bipolar cells. J Comp Neurol 396:351–365
Flores-Herr N, Protti DA, Wässle H (2001) Synaptic currents generating the inhibitory surround of ganglion cells in the mammalian retina. J Neurosci 21:4852–4863
Freed MA, Smith RG, Sterling P (2003) Timing of quantal release from the retinal bipolar terminal is regulated by a feedback circuit. Neuron 38:89–101
Hartmann K, Stief F, Draguhn A, Frahm C (2004) Ionotropic GABA receptors with mixed pharmacological properties of GABAA and GABAC receptors. Eur J Pharmacol 197:139–146
Hartveit E (1999) Reciprocal synaptic interactions between rod bipolar cells and amacrine cells in the rat retina. J Neurophysiol 81:2923–2936
Ichinose T, Lukasiewicz PD (2005) Inner and outer retinal pathways both contribute to surround inhibition of salamander ganglion cells. J Physiol 565:517–535
Ishikane H, Gangi M, Honda S, Tachibana M (2005) Synchronized retinal oscillations encode essential information for escape behavior in frogs. Nat Neurosci 8:1087–1095
Jacobs AL, Werblin FS (1998) Spatiotemporal patterns at the retinal output. J Neurophysiol 80:447–451
Johnston GA, Curtis DR, Beart PM, Game CJ, McCulloch RM, Twitchin B (1975) Cis- and trans-4-aminocrotonic acid as GABA analogues of restricted conformation. J Neurochem 24:157–160
Kamermans M, Werblin F (1992) GABA-mediated positive autofeedback loop controls horizontal cell kinetics in tiger salamander retina. J Neurosci 12:2451–2463
Kirischuk S, Akyeli J, Iosub R, Grantyn R (2003) Pre- and postsynaptic contribution of GABAC receptors to GABAergic synaptic transmission in rat collicular slices and cultures. Eur J Neurosci 18:752–758
Koulen P, Brandstätter JH, Kröger S, Enz R, Bormann J, Wässle H (1997) Immunocytochemical localization of the GABAC receptor ρ subunits in the cat, goldfish, and chicken retina. J Comp Neurol 380:520–532
Koulen P, Brandstätter JH, Enz R, Bormann J, Wässle H (1998) Synaptic clustering of GABAC receptor ρ-subunits in the rat retina. Eur J Neurosci 10:115–127
Lukasiewicz PD, Maple BR, Werblin FS (1994) A novel GABA receptor on bipolar cell terminals in the tiger salamander retina. J Neurosci 14:1201–1212
Lukasiewicz PD (1996) GABAC receptors in the vertebrate retina. Mol Neurobiol 12:181–194
Lukasiewicz PD, Eggers ED, Sagdullaev BT, McCall MA (2004) GABAC receptor-mediated inhibition in the retina. Vision Res 44:3289–3296
Matsui K, Hasegawa J, Tachibana M (2001) Modulation of excitatory synaptic transmission by GABAC receptor-mediated feedback in the mouse inner retina. J Neurophysiol 86:2285–2298
McCall MA, Lukasiewicz PD, Gregg RG, Peachey NS (2002) Elimination of the ρ1 subunit abolishes GABAC receptor expression and alters visual processing in the mouse retina. J Neurosci 22:4163–4174
McGillem GS, Rotolo TC, Dacheux RF (2000) GABA responses of rod bipolar cells in rabbit retinal slices. Vis Neurosci 17:381–389
Nawy S, Jahr CE (1990) Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells. Nature 346:269–271
Ogurusu T, Yanagi K, Watanabe M, Fukaya M, Shingai R (1999) Localization of GABA receptor ρ2 and ρ3 subunits in rat brain and functional expression of homooligomeric ρ3 receptors and heterooligomeric ρ2 ρ3 receptors. Receptors Channels 6:463–475
Paik SS, Park NG, Lee SJ, Han HK, Jung CS, Bai SH, Chun MH (2003) GABA receptors on horizontal cells in the goldfish retina. Vision Res 43:2101–2106
Pan ZH, Lipton SA (1995) Multiple GABA receptor subtypes mediate inhibition of calcium influx at rat retinal bipolar cell terminals. J Neurosci 15:2668–2679
Pasternack M, Boller M, Pau B, Schmidt M (1999) GABAA and GABAC receptors have contrasting effects on excitability in superior colliculus. J Neurophysiol 82:2020–2023
Picaud S, Pattnaik B, Hicks D, Forster V, Fontaine V, Sahel J, Dreyfus H (1998) GABAA and GABAC receptors in adult porcine cones: evidence from a photoreceptor-glia co-culture model. J Physiol 513:33–42
Platt B, Withington DJ (1998) GABA-induced long-term potentiation in the guinea-pig superior colliculus. Neuropharmacology 37:1111–1122
Qian H, Dowling JE (1993) Novel GABA responses from rod-driven retinal horizontal cells. Nature 361:162–164
Qian H, Dowling JE (1994) Pharmacology of novel GABA receptors found on rod horizontal cells of the white perch retina. J Neurosci 14:4299–4307
Qian H, Dowling JE (1995) GABAA and GABAC receptors on hybrid bass retinal bipolar cells. J Neurophysiol 74:1920–1928
Qian H (2000) GABAC receptors in the vertebrate retina. Webvision, University of Utah, available online at http://www.webvision.med.utah.edu/GABA-C.htm , last visited: 9 May 2007
Roska B, Nemeth E, Werblin FS (1998) Response to change is facilitated by a three-neuron disinhibitory pathway in the tiger salamander retina. J Neurosci 18:3451–3459
Roska B, Nemeth E, Orzo L, Werblin FS (2000) Three levels of lateral inhibition: A space-time study of the retina of the tiger salamander. J Neurosci 20:1941–1951
Rozzo A, Ballerini L, Nistri A (1999) Antagonism by (1,2,5,6-tetrahydropyridine-4-yl) methylphosphinic acid of synaptic transmission in the neonatal rat spinal cord in vitro: an electrophysiological study. Neuroscience 90:1085–1092
Rozzo A, Armellin M, Franzot J, Chiaruttini C, Nistri A, Tongiorgi E (2002) Expression and dendritic mRNA localization of GABAC receptor ρ1 and ρ2 subunits in developing rat brain and spinal cord. Eur J Neurosci 15:1747–1758
Schlicker K, Boller M, Schmidt M (2004) GABAC receptor mediated inhibition in acutely isolated neurons of the rat dorsal lateral geniculate nucleus. Brain Res Bull 63:91–97
Schlicker K, Schmidt M (2005) Intrinsic organization of the medial terminal nucleus in mice: an electrophysiological and pharmacological study in vitro. Soc Neurosci Abstr 35:507.5p
Schnapf JL, Copenhagen DR (1982) Differences in the kinetics of rod and cone synaptic transmission. Nature 296:862–864
Schmidt M (1997) GABAC receptors contribute to inhibitory circuits in the rat subcortical visual system. Soc Neurosci Abstr 23:172p
Schmidt M, Boller M, Özen G, Hall WC (2001) Disinhibition in rat superior colliculus mediated by GABAC receptors. J Neurosci 21:691–699
Semyanov A, Kullmann DM (2002) Relative picrotoxin insensitivity distinguishes ionotropic GABA receptor-mediated IPSCs in hippocampal interneurons. Neuropharmacology 43:726–736
Shen W, Slaughter MM (2001) Multireceptor GABAergic regulation of synaptic communication in amphibian retina. J Physiol 530:55–67
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
Slaughter MM, Miller RF (1981) 2-Amino-4-phosphonobutyric acid: a new pharmacological tool for retina research. Science 211:182–185
Strata F, Cherubini E (1994) Transient expression of a novel type of GABA response in rat CA3 hippocampal neurones during development. J Physiol 480:493–503
Vaquero CF, de la Villa P (1999) Localisation of the GABAC receptors at the axon terminal of the rod bipolar cells of the mouse retina. Neurosci Res 35:1–7
Wall MJ (2001) cis-4-Amino-crotonic acid activates α6 subunit-containing GABAA but not GABAC receptors in granule cells of adult rat cerebellar slices. Neurosci Lett 316:37–40
Wegelius K, Pasternack M, Hiltunen JO, Rivera C, Kaila K, Saarma M, Reeben M (1998) Distribution of GABA receptor ρ subunit transcripts in the rat brain. Eur J Neurosci 10:350–357
Wellis DP, Werblin FS (1995) Dopamine modulates GABAC receptors mediating inhibition of calcium entry into and transmitter release from bipolar cell terminals in tiger salamander retina. J Neurosci 15:4748–4761
White AM, Platt B (2001) Ionic mechanisms of GABA-induced long-term potentiation in the rat superior colliculus. Exp Brain Res 140:486–494
Zhang J, Slaughter MM (1995) Preferential suppression of the ON pathway by GABAC receptors in the amphibian retina. J Neurophysiol 74:1583–1592
Zhang J, Jung CS, Slaughter MM (1997) Serial inhibitory synapses in retina. Vis Neurosci 14:553–563
Zhu JJ, Lo FS (1999) Three GABA receptor-mediated postsynaptic potentials in interneurons in the rat lateral geniculate nucleus. J Neurosci 19:5721–5730
Author information
Authors and Affiliations
Corresponding author
Editor information
Rights and permissions
Copyright information
© 2007 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Schmidt, M. (2007). GABAC Receptors in Retina and Brain. In: Darlison, M.G. (eds) Inhibitory Regulation of Excitatory Neurotransmission. Results and Problems in Cell Differentiation, vol 44. Springer, Berlin, Heidelberg. https://doi.org/10.1007/400_2007_031
Download citation
DOI: https://doi.org/10.1007/400_2007_031
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-540-72601-2
Online ISBN: 978-3-540-72602-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)