GABAA,slow: Causes and consequences

Trends in Neurosciences

Volumn 34, Issue 2, 2011, Pages 101-112

  Capogna, Marco ^a   Pearce, Robert A ^b  

^a MRC Anat Neuropharmacology Unit   (United Kingdom)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; RECEPTOR SUBUNIT;

CELL KINETICS; CELL TYPE; GABAERGIC SYSTEM; HIPPOCAMPUS; INTERNEURON; OSCILLATION; PRIORITY JOURNAL; REVIEW; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION;

ANIMALS; DRUG DESIGN; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; HUMANS; NEURAL INHIBITION; NEURONS; PROTEIN SUBUNITS; RECEPTORS, GABA-A; SYNAPSES; SYNAPTIC TRANSMISSION; TIME FACTORS;

EID: 79551611534     PISSN: 01662236     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tins.2010.10.005     Document Type: Review

References (120)

1. Coombs J.S., et al. The specific ionic conductances and the ionic movements across the motoneuronal membrane that produce the inhibitory post-synaptic potential. J. Physiol. 1955, 130:326-374.
2. Farrant M., Nusser Z. Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat. Rev. Neurosci. 2005, 6:215-229.
3. Kaneda M., et al. Whole-cell and single-channel currents activated by GABA and glycine in granule cells of the rat cerebellum. J. Physiol. 1995, 485:419-435.
4. Pearce R.A. Physiological evidence for two distinct GABAA responses in rat hippocampus. Neuron 1993, 10:189-200.
5. Kapur A., et al. GABAA-mediated IPSCs in piriform cortex have fast and slow components with different properties and locations on pyramidal cells. J. Neurophysiol. 1997, 78:2531-2545.
6. Sceniak M.P., Maciver M.B. Slow GABA(A) mediated synaptic transmission in rat visual cortex. BMC Neurosci. 2008, 9:8.
7. Tamas G., et al. Identified sources and targets of slow inhibition in the neocortex. Science 2003, 299:1902-1905.
8. Huntsman M.M., et al. Reciprocal inhibitory connections and network synchrony in the mammalian thalamus. Science 1999, 283:541-543.
9. Schofield C.M., Huguenard J.R. GABA affinity shapes IPSCs in thalamic nuclei. J. Neurosci. 2007, 27:7954-7962.
10. - currents in rat thalamic reticular and relay neurons. J. Neurophysiol. 1997, 78:2280-2286.
11. Rossi D.J., Hamann M. Spillover-mediated transmission at inhibitory synapses promoted by high affinity alpha6 subunit GABA(A) receptors and glomerular geometry. Neuron 1998, 20:783-795.
12. Crowley J.J., et al. Dynamics of fast and slow inhibition from cerebellar Golgi cells allow flexible control of synaptic integration. Neuron 2009, 63:843-853.
13. Delaney A.J., Sah P. Pathway-specific targeting of GABA(A) receptor subtypes to somatic and dendritic synapses in the central amygdala. J. Neurophysiol. 2001, 86:717-723.
14. Geracitano R., et al. Synaptic heterogeneity between mouse paracapsular intercalated neurons of the amygdala. J. Physiol. 2007, 585:117-134.
15. Kuo S.P., et al. Heterogeneous kinetics and pharmacology of synaptic inhibition in the chick auditory brainstem. J. Neurosci. 2009, 29:9625-9634.
16. Bacci A., et al. Major differences in inhibitory synaptic transmission onto two neocortical interneuron subclasses. J. Neurosci. 2003, 23:9664-9674.
17. Hajos N., Mody I. Synaptic communication among hippocampal interneurons: properties of spontaneous IPSCs in morphologically identified cells. J. Neurosci. 1997, 17:8427-8442.
18. Houston C.M., et al. Intracellular chloride ions regulate the time course of GABA-mediated inhibitory synaptic transmission. J. Neurosci. 2009, 29:10416-10423.
19. Otis T.S., Mody I. Modulation of decay kinetics and frequency of GABAA receptor-mediated spontaneous inhibitory postsynaptic currents in hippocampal neurons. Neuroscience 1992, 49:13-32.
20. Edwards F.A., et al. Quantal analysis of inhibitory synaptic transmission in the dentate gyrus of rat hippocampal slices: a patch-clamp study. J. Physiol. 1990, 430:213-249.
21. Nusser Z., et al. Differential regulation of synaptic GABAA receptors by cAMP-dependent protein kinase in mouse cerebellar and olfactory bulb neurones. J. Physiol. 1999, 521:421-435.
22. Ouardouz M., Lacaille J.C. Properties of unitary IPSCs in hippocampal pyramidal cells originating from different types of interneurons in young rats. J. Neurophysiol. 1997, 77:1939-1949.
23. Banks M.I., et al. The synaptic basis of GABAA,slow. J. Neurosci. 1998, 18:1305-1317.
24. Pearce R.A. Volatile anaesthetic enhancement of paired-pulse depression investigated in the rat hippocampus in vitro. J. Physiol. 1996, 492:823-840.
25. Banks M.I., et al. Development of GABA(A) receptor-mediated inhibitory postsynaptic currents in hippocampus. J. Neurophysiol. 2002, 88:3097-3107.
26. Klausberger T., Somogyi P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 2008, 321:53-57.
27. Megias M., et al. Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 2001, 102:527-540.
28. Olah S., et al. Regulation of cortical microcircuits by unitary GABA-mediated volume transmission. Nature 2009, 461:1278-1281.
29. Olah S., et al. Output of neurogliaform cells to various neuron types in the human and rat cerebral cortex. Front. Neural Circuits 2007, 1:4.
30. Szabadics J., et al. Different transmitter transients underlie presynaptic cell type specificity of GABAA,slow and GABAA,fast. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:14831-14836.
31. Price C.J., et al. Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area. J. Neurosci. 2005, 25:6775-6786.
32. Price C.J., et al. GABA(B) receptor modulation of feedforward inhibition through hippocampal neurogliaform cells. J. Neurosci. 2008, 28:6974-6982.
33. Fuentealba P., et al. Ivy cells: a population of nitric-oxide-producing, slow-spiking GABAergic neurons and their involvement in hippocampal network activity. Neuron 2008, 57:917-929.
34. Ramon y Cajal S. Estructura del asta de Ammon y fascia dentata. Anal. Soc. Espan. Hist. Nat. 1893, 22:53-114.
35. Valverde F. Short axon neuronal subsystems in the visual cortex of the monkey. Int. J. Neurosci. 1971, 1:181-197.
36. Jones E.G. Varieties and distribution of non-pyramidal cells in the somatic sensory cortex of the squirrel monkey. J. Comp. Neurol. 1975, 160:205-267.
37. Kisvarday Z.F., et al. Synapses, axonal and dendritic patterns of GABA-immunoreactive neurons in human cerebral cortex. Brain 1990, 113:793-812.
38. Hestrin S., Armstrong W.E. Morphology and physiology of cortical neurons in layer I. J. Neurosci. 1996, 16:5290-5300.
39. Kawaguchi Y., Kubota Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex 1997, 7:476-486.
40. Vida I., et al. Unitary IPSPs evoked by interneurons at the stratum radiatum-stratum lacunosum-moleculare border in the CA1 area of the rat hippocampus in vitro. J. Physiol. 1998, 506:755-773.
41. Khazipov R., et al. Hippocampal CA1 lacunosum-moleculare interneurons: modulation of monosynaptic GABAergic IPSCs by presynaptic GABAB receptors. J. Neurophysiol. 1995, 74:2126-2137.
42. Karayannis T., et al. Slow GABA transient and receptor desensitization shape synaptic responses evoked by hippocampal neurogliaform cells. J. Neurosci. 2010, 30:9898-9909.
43. Wei W., et al. Perisynaptic localization of delta subunit-containing GABA(A) receptors and their activation by GABA spillover in the mouse dentate gyrus. J. Neurosci. 2003, 23:10650-10661.
44. Fuentealba P., et al. Expression of COUP-TFII nuclear receptor in restricted GABAergic neuronal populations in the adult rat hippocampus. J. Neurosci. 2010, 30:1595-1609.
45. Szabadics J., Soltesz I. Functional specificity of mossy fiber innervation of GABAergic cells in the hippocampus. J. Neurosci. 2009, 29:4239-4251.
46. Tricoire L., et al. Common origins of hippocampal Ivy and nitric oxide synthase expressing neurogliaform cells. J. Neurosci. 2010, 30:2165-2176.
47. Amano T., et al. Synaptic correlates of fear extinction in the amygdala. Nat. Neurosci. 2010, 13:489-494.
48. Farrant M., Kaila K. The cellular, molecular and ionic basis of GABA(A) receptor signalling. Prog. Brain Res. 2007, 160:59-87.
49. Hentschke H., et al. Altered GABAA,slow inhibition and network oscillations in mice lacking the GABAA receptor beta3 subunit. J. Neurophysiol. 2009, 102:3643-3655.
50. Ju Y.H., et al. Distinct properties of murine alpha 5 gamma-aminobutyric acid type a receptors revealed by biochemical fractionation and mass spectroscopy. J. Neurosci. Res 2009, 87:1737-1747.
51. Caraiscos V.B., et al. Tonic inhibition in mouse hippocampal CA1 pyramidal neurons is mediated by alpha5 subunit-containing gamma-aminobutyric acid type A receptors. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:3662-3667.
52. Scimemi A., et al. Multiple and plastic receptors mediate tonic GABAA receptor currents in the hippocampus. J. Neurosci. 2005, 25:10016-10024.
53. Prenosil G.A., et al. Specific subtypes of GABAA receptors mediate phasic and tonic forms of inhibition in hippocampal pyramidal neurons. J. Neurophysiol. 2006, 96:846-857.
54. Glykys J., Mody I. Hippocampal network hyperactivity after selective reduction of tonic inhibition in GABA A receptor alpha5 subunit-deficient mice. J. Neurophysiol. 2006, 95:2796-2807.
55. Zarnowska E.D., et al. GABAA receptor alpha5 subunits contribute to GABAA,slow synaptic inhibition in mouse hippocampus. J. Neurophysiol. 2009, 101:1179-1191.
56. Vargas-Caballero M., et al. alpha5 Subunit-containing GABA(A) receptors mediate a slowly decaying inhibitory synaptic current in CA1 pyramidal neurons following Schaffer collateral activation. Neuropharmacology 2010, 58:668-675.
57. Ali A.B., Thomson A.M. Synaptic alpha 5 subunit-containing GABAA receptors mediate IPSPs elicited by dendrite-preferring cells in rat neocortex. Cereb. Cortex 2008, 18:1260-1271.
58. Vicini S., et al. GABA(A) receptor alpha1 subunit deletion prevents developmental changes of inhibitory synaptic currents in cerebellar neurons. J. Neurosci. 2001, 21:3009-3016.
59. Isaacson J.S., et al. Local and diffuse synaptic actions of GABA in the hippocampus. Neuron 1993, 10:165-175.
60. Barberis A., et al. Presynaptic source of quantal size variability at GABAergic synapses in rat hippocampal neurons in culture. Eur. J. Neurosci. 2004, 20:1803-1810.
61. Nusser Z., et al. Synapse-specific contribution of the variation of transmitter concentration to the decay of inhibitory postsynaptic currents. Biophys. J. 2001, 80:1251-1261.
62. Vizi E.S., et al. Non-synaptic receptors and transporters involved in brain functions and targets of drug treatment. Br. J. Pharmacol. 2010, 160:785-809.
63. Zsiros V., Maccaferri G. Electrical coupling between interneurons with different excitable properties in the stratum lacunosum-moleculare of the juvenile CA1 rat hippocampus. J. Neurosci. 2005, 25:8686-8695.
64. Stuart G. Voltage-activated sodium channels amplify inhibition in neocortical pyramidal neurons. Nat. Neurosci. 1999, 2:144-150.
65. Hardie J.B., Pearce R.A. Active and passive membrane properties and intrinsic kinetics shape synaptic inhibition in hippocampal CA1 pyramidal neurons. J. Neurosci. 2006, 26:8559-8569.
66. Bellingham M.C., et al. Developmental changes in EPSC quantal size and quantal content at a central glutamatergic synapse in rat. J. Physiol. 1998, 511:861-869.
67. Cathala L., et al. Changes in synaptic structure underlie the developmental speeding of AMPA receptor-mediated EPSCs. Nat. Neurosci. 2005, 8:1310-1318.
68. Esposito M.S., et al. Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J. Neurosci. 2005, 25:10074-10086.
69. Markwardt S.J., et al. Input-specific GABAergic signaling to newborn neurons in adult dentate gyrus. J. Neurosci. 2009, 29:15063-15072.
70. Balakrishnan V., et al. Slow glycinergic transmission mediated by transmitter pooling. Nat. Neurosci. 2009, 12:286-294.
71. Hefft S., Jonas P. Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat. Neurosci. 2005, 8:1319-1328.
72. Lu T., Trussell L.O. Inhibitory transmission mediated by asynchronous transmitter release. Neuron 2000, 26:683-694.
73. Sohal V.S., et al. Reciprocal inhibitory connections regulate the spatiotemporal properties of intrathalamic oscillations. J. Neurosci. 2000, 20:1735-1745.
74. Huntsman M.M., Huguenard J.R. Fast IPSCs in rat thalamic reticular nucleus require the GABAA receptor beta1 subunit. J. Physiol. 2006, 572:459-475.
75. Kanter E.D., et al. A dendritic GABAA-mediated IPSP regulates facilitation of NMDA-mediated responses to burst stimulation of afferent fibers in piriform cortex. J. Neurosci. 1996, 16:307-312.
76. Witter M.P., et al. Entorhinal projections to the hippocampal CA1 region in the rat: an underestimated pathway. Neurosci. Lett. 1988, 85:193-198.
77. Miles R., et al. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 1996, 16:815-823.
78. 2+]i changes in the dendrites of hippocampal CA1 pyramidal neurons. J. Neurophysiol. 1996, 76:2896-2906.
79. Pearce R.A., et al. Different mechanisms for use-dependent depression of two GABAA-mediated IPSCs in rat hippocampus. J. Physiol. 1995, 484:425-435.
80. Mott D.D., et al. Baclofen facilitates the development of long-term potentiation in the rat dentate gyrus. Neurosci. Lett. 1990, 113:222-226.
81. Buzsaki G. Theta oscillations in the hippocampus. Neuron 2002, 33:325-340.
82. Bragin A., et al. Gamma (40-100Hz) oscillation in the hippocampus of the behaving rat. J. Neurosci. 1995, 15:47-60.
83. Gray C.M., Singer W. Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc. Natl. Acad. Sci. U. S. A. 1989, 86:1698-1702.
84. Sejnowski T.J., Paulsen O. Network oscillations: emerging computational principles. J. Neurosci. 2006, 26:1673-1676.
85. Winson J. Patterns of hippocampal theta rhythm in the freely moving rat. Electroencephalogr. Clin. Neurophysiol. 1974, 36:291-301.
86. Elfant D., et al. Specific inhibitory synapses shift the balance from feedforward to feedback inhibition of hippocampal CA1 pyramidal cells. Eur. J. Neurosci. 2008, 27:104-113.
87. Chapman C.A., Lacaille J.C. Intrinsic theta-frequency membrane potential oscillations in hippocampal CA1 interneurons of stratum lacunosum-moleculare. J. Neurophysiol. 1999, 81:1296-1307.
88. Tort A.B., et al. On the formation of gamma-coherent cell assemblies by oriens lacunosum-moleculare interneurons in the hippocampus. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:13490-13495.
89. Holsheimer J., et al. The double dipole model of theta rhythm generation: simulation of laminar field potential profiles in dorsal hippocampus of the rat. Brain Res. 1982, 235:31-50.
90. Banks M.I., et al. Interactions between distinct GABA(A) circuits in hippocampus. Neuron 2000, 25:449-457.
91. Steward O., Scoville S.A. Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J. Comp. Neurol. 1976, 169:347-370.
92. Colbert C.M., Levy W.B. Electrophysiological and pharmacological characterization of perforant path synapses in CA1: mediation by glutamate receptors. J. Neurophysiol. 1992, 68:1-8.
93. Soltesz I., Deschenes M. Low- and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of the rat hippocampus under ketamine-xylazine anesthesia. J. Neurophysiol. 1993, 70:97-116.
94. Empson R.M., Heinemann U. Perforant path connections to area CA1 are predominantly inhibitory in the rat hippocampal-entorhinal cortex combined slice preparation. Hippocampus 1995, 5:104-107.
95. Kamondi A., et al. Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus 1998, 8:244-261.
96. Csicsvari J., et al. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving Rat. J. Neurosci. 1999, 19:274-287.
97. White J.A., et al. Networks of interneurons with fast and slow gamma-aminobutyric acid type A (GABAA) kinetics provide substrate for mixed gamma-theta rhythm. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:8128-8133.
98. Hasselmo M.E., et al. A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput. 2002, 14:793-817.
99. Franks N.P. General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal. Nat. Rev. Neurosci. 2008, 9:370-386.
100. Banks M.I., Pearce R.A. Dual actions of volatile anesthetics on GABA(A) IPSCs: dissociation of blocking and prolonging effects. Anesthesiology 1999, 90:120-134.
101. Gage P.W., Robertson B. Prolongation of inhibitory postsynaptic currents by pentobarbitone, halothane and ketamine in CA1 pyramidal cells in rat hippocampus. Br. J. Pharmacol. 1985, 85:675-681.
102. Antkowiak B., Heck D. Effects of the volatile anesthetic enflurane on spontaneous discharge rate and GABA(A)-mediated inhibition of Purkinje cells in rat cerebellar slices. J. Neurophysiol. 1997, 77:2525-2538.
103. Lukatch H.S., MacIver M.B. Voltage-clamp analysis of halothane effects on GABA(A fast) and GABA(A slow) inhibitory currents. Brain Res. 1997, 765:108-112.
104. Dai S., et al. Amnestic concentrations of etomidate modulate GABAA,slow synaptic inhibition in hippocampus. Anesthesiology 2009, 111:766-773.
105. MacIver M.B. Abused inhalants enhance GABA-mediated synaptic inhibition. Neuropsychopharmacology 2009, 34:2296-2304.
106. Collinson N., et al. Enhanced learning and memory and altered GABAergic synaptic transmission in mice lacking the alpha 5 subunit of the GABAA receptor. J. Neurosci. 2002, 22:5572-5580.
107. Crestani F., et al. Trace fear conditioning involves hippocampal alpha5 GABA(A) receptors. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:8980-8985.
108. Martin L.J., et al. The physiological properties and therapeutic potential of alpha5-GABAA receptors. Biochem. Soc. Trans. 2009, 37:1334-1337.
109. Ballard T.M., et al. RO4938581, a novel cognitive enhancer acting at GABAA alpha5 subunit-containing receptors. Psychopharmacology (Berl.) 2009, 202:207-223.
110. Howell O., et al. Density and pharmacology of alpha5 subunit-containing GABA(A) receptors are preserved in hippocampus of Alzheimer's disease patients. Neuroscience 2000, 98:669-675.
111. Johnston D., Brown T.H. Interpretation of voltage-clamp measurements in hippocampal neurons. J. Neurophysiol. 1983, 50:464-486.
112. Spruston N., et al. Voltage- and space-clamp errors associated with the measurement of electrotonically remote synaptic events. J. Neurophysiol. 1993, 70:781-802.
113. Williams S.R., Mitchell S.J. Direct measurement of somatic voltage clamp errors in central neurons. Nat. Neurosci. 2008, 11:790-798.
114. Golding N.L., et al. Factors mediating powerful voltage attenuation along CA1 pyramidal neuron dendrites. J. Physiol. 2005, 568:69-82.
115. Spruston N. Pyramidal neurons: dendritic structure and synaptic integration. Nat. Rev. Neurosci. 2008, 9:206-221.
116. Hausser M., Roth A. Estimating the time course of the excitatory synaptic conductance in neocortical pyramidal cells using a novel voltage jump method. J. Neurosci. 1997, 17:7606-7625.
117. Maccaferri G., et al. Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro. J. Physiol. 2000, 524:91-116.
118. Jacob T.C., et al. GABA(A) receptor trafficking and its role in the dynamic modulation of neuronal inhibition. Nat. Rev. Neurosci. 2008, 9:331-343.
119. Canepari M., et al. Imaging inhibitory synaptic potentials using voltage sensitive dyes. Biophys. J. 2010, 98:2032-2040.
120. Cauli B., et al. Cortical GABA interneurons in neurovascular coupling: relays for subcortical vasoactive pathways. J. Neurosci. 2004, 24:8940-8949.