Coincident pre- and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cl- transporter activity

Neuron

Volumn 39, Issue 5, 2003, Pages 807-820

  Woodin, Melanie A ^a   Ganguly, Karunesh ^a,b   Poo, Mu ming ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL;

ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN SLICE; CONTROLLED STUDY; EMBRYO; GABAERGIC SYSTEM; HIPPOCAMPUS; NEUROMODULATION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT;

EID: 0042028516     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(03)00507-5     Document Type: Article

References (66)

1. Abbott L.F. Integrating with action potentials. Neuron. 26:2000;3-4.
2. Aizenman C.D., Manis P.B., Linden D.J. Polarity of long-term synaptic gain change is related to postsynaptic spike firing at a cerebellar inhibitory synapse. Neuron. 21:1998;827-835.
3. Bazhenov M., Timofeev I., Steriade M., Sejnowski T.J. Self-sustained rhythmic activity in the thalamic reticular nucleus mediated by depolarizing GABAA receptor potentials. Nat. Neurosci. 2:1999;168-174.
4. Bi G.Q., Poo M.M. Synaptic modifications in cultured hippocampal neurons. dependence on spike timing, synaptic strength, and postsynaptic cell type J. Neurosci. 18:1998;10464-10472.
5. Bi G., Poo M. Synaptic modification by correlated activity. Hebb's postulate revisited Annu. Rev. Neurosci. 24:2001;139-166.
6. Bliss T.V., Collingridge G.L. A synaptic model of memory. long-term potentiation in the hippocampus Nature. 361:1993;31-39.
7. Bliss T.V., Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232:1973;331-356.
8. Cabantchik Z.I., Greger R. Chemical probes for anion transporters of mammalian cell membranes. Am. J. Physiol. 262:1992;C803-C827.
9. Callaway J.C., Ross W.N. Frequency-dependent propagation of sodium action potentials in dendrites of hippocampal CA1 pyramidal neurons. J. Neurophysiol. 74:1995;1395-1403.
10. Carroll R.C., Lissin D.V., von Zastrow M., Nicoll R.A., Malenka R.C. Rapid redistribution of glutamate receptors contributes to long-term depression in hippocampal cultures. Nat. Neurosci. 2:1999;454-460.
11. Chen G., Trombley P.Q., van den Pol A.N. Excitatory actions of GABA in developing rat hypothalamic neurones. J. Physiol. 494:1996;451-464.
12. Collin C., Devane W.A., Dahl D., Lee C.J., Axelrod J., Alkon D.L. Long-term synaptic transformation of hippocampal CA1 gamma-aminobutyric acid synapses and the effect of anandamide. Proc. Natl. Acad. Sci. USA. 92:1995;10167-10171.
13. Debanne D., Gahwiler B.H., Thompson S.M. Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. J. Physiol. 507:1998;237-247.
14. Feldman D.E. Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron. 27:2000;45-56.
15. Fitzsimonds R.M., Song H.J., Poo M.M. Propagation of activity-dependent synaptic depression in simple neural networks. Nature. 388:1997;439-448.
16. Frech M.J., Deitmer J.W., Backus K.H. Intracellular chloride and calcium transients evoked by gamma-aminobutyric acid and glycine in neurons of the rat inferior colliculus. J. Neurobiol. 40:1999;386-396.
17. Froemke R.C., Dan Y. Spike-timing-dependent synaptic modification induced by natural spike trains. Nature. 416:2002;433-438.
18. Ganguly K., Schinder A.F., Wong S.T., Poo M. GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell. 105:2001;521-532.
19. Hayashi Y., Shi S.H., Esteban J.A., Piccini A., Poncer J.C., Malinow R. Driving AMPA receptors into synapses by LTP and CaMKII. requirement for GluR1 and PDZ domain interaction Science. 287:2000;2262-2267.
20. Hebb D.O. The Organization of Behavior. 1949;Wiley Interscience, New York.
21. + channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature. 387:1997;869-875.
22. Hopfield J.J. Pattern recognition computation using action potential timing for stimulus representation. Nature. 376:1995;33-36.
23. Hubner C.A., Stein V., Hermans-Borgmeyer I., Meyer T., Ballanyi K., Jentsch T.J. Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition. Neuron. 30:2001;515-524.
24. Jarolimek W., Lewen A., Misgeld U. A furosemide-sensitive K+-Cl- cotransporter counteracts intracellular Cl- accumulation and depletion in cultured rat midbrain neurons. J. Neurosci. 19:1999;4695-4704.
25. Kakazu Y., Akaike N., Komiyama S., Nabekura J. Regulation of intracellular chloride by cotransporters in developing lateral superior olive neurons. J. Neurosci. 19:1999;2843-2851.
26. Kano M., Rexhausen U., Dreessen J., Konnerth A. Synaptic excitation produces a long-lasting rebound potentiation of inhibitory synaptic signals in cerebellar Purkinje cells. Nature. 356:1992;601-604.
27. Katz L.C., Shatz C.J. Synaptic activity and the construction of cortical circuits. Science. 274:1996;1133-1138.
28. Kelsch W., Hormuzdi S., Straube E., Lewen A., Monyer H., Misgeld U. Insulin-like growth factor 1 and a cytosolic tyrosine kinase activate chloride outward transport during maturation of hippocampal neurons. J. Neurosci. 21:2001;8339-8347.
29. Klausberger T., Magill P.J., Marton L.F., Roberts J.D., Cobden P.M., Buzsaki G., Somogyi P. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature. 421:2003;844-848.
30. Koester H.J., Sakmann B. Calcium dynamics in single spines during coincident pre- and postsynaptic activity depend on relative timing of back-propagating action potentials and subthreshold excitatory postsynaptic potentials. Proc. Natl. Acad. Sci. USA. 95:1998;9596-9601.
31. Komatsu Y. GABAB receptors, monoamine receptors, and postsynaptic inositol trisphosphate-induced Ca2+ release are involved in the induction of long-term potentiation at visual cortical inhibitory synapses. J. Neurosci. 16:1996;6342-6352.
32. Komatsu Y., Iwakiri M. Long-term modification of inhibitory synaptic transmission in developing visual cortex. Neuroreport. 4:1993;907-910.
33. Kyrozis A., Reichling D.B. Perforated-patch recording with gramicidin avoids artifactual changes in intracellular chloride concentration. J. Neurosci. Methods. 57:1995;27-35.
34. Lee H.-K., Kameyama K., Huganir R.L., Bear M.F. NMDA induces long-term synaptic depression and dephosphorylation of the GluR1 subunit of AMPA receptors in the hippocampus. Neuron. 21:1998;1151-1162.
35. Ling D.S., Benardo L.S. Activity-dependent depression of monosynaptic fast IPSCs in hippocampus. contributions from reductions in chloride driving force and conductance Brain Res. 670:1995;142-146.
36. Lu J., Karadsheh M., Delpire E. Developmental regulation of the neuronal-specific isoform of K-Cl cotransporter KCC2 in postnatal rat brains. J. Neurobiol. 39:1999;558-568.
37. Maccaferri G., Roberts J.D., Szucs P., Cottingham C.A., Somogyi P. Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro. J. Physiol. 524:2000;91-116.
38. Magee J.C., Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science. 275:1997;209-213.
39. Malenka R.C., Nicoll R.A. NMDA-receptor-dependent synaptic plasticity. multiple forms and mechanisms Trends Neurosci. 16:1993;521-527.
40. Markram H., Lubke J., Frotscher M., Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science. 275:1997;213-215.
41. Martin S.J., Grimwood P.D., Morris R.G.M. Synaptic plasticity and memory. An evaluation of the hypothesis Annu. Rev. Neurosci. 23:2000;649-711.
42. Marty A., Llano I. Modulation of inhibitory synapses in the mammalian brain. Curr. Opin. Neurobiol. 5:1995;335-341.
43. McBain C.J., Fisahn A. Interneurons unbound. Nat. Rev. Neurosci. 2:2001;11-23.
44. McLean H.A., Caillard O., Ben Ari Y., Gaiarsa J.L. Bidirectional plasticity expressed by GABAergic synapses in the neonatal rat hippocampus. J. Physiol. 496:1996;471-477.
45. Miles R., Toth K., Gulyas A.I., Hajos N., Freund T.F. Differences between somatic and dendritic inhibition in the hippocampus. Neuron. 16:1996;815-823.
46. Misgeld U., Deisz R.A., Dodt H.U., Lux H.D. The role of chloride transport in postsynaptic inhibition of hippocampal neurons. Science. 232:1986;1413-1415.
47. Nicoll R.A., Malenka R.C. Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature. 377:1995;115-118.
48. Nusser Z., Hajos N., Somogyi P., Mody I. Increased number of synaptic GABA(A) receptors underlies potentiation at hippocampal inhibitory synapses. Nature. 395:1998;172-177.
49. Owens D.F., Boyce L.H., Davis M.B., Kriegstein A.R. Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J. Neurosci. 16:1996;6414-6423.
50. Payne J.A., Stevenson T.J., Donaldson L.F. Molecular characterization of a putative K-Cl cotransporter in rat brain. A neuronal-specific isoform. J. Biol. Chem. 271:1996;16245-16252.
51. Plotkin M.D., Snyder E.Y., Hebert S.C., Delpire E. Expression of the Na-K-2Cl cotransporter is developmentally regulated in postnatal rat brains. a possible mechanism underlying GABA's excitatory role in immature brain J. Neurobiol. 33:1997;781-795.
52. Rivera C., Voipio J., Payne J.A., Ruusuvuori E., Lahtinen H., Lamsa K., Pirvola U., Saarma M., Kaila K. The K+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature. 397:1999;251-255.
53. Rohrbough J., Spitzer N.C. Regulation of intracellular Cl- levels by Na(+)-dependent Cl- cotransport distinguishes depolarizing from hyperpolarizing GABAA receptor-mediated responses in spinal neurons. J. Neurosci. 16:1996;82-91.
54. Schoepfle G.M., Erlanger J. The action of temperature on the excitability, spike height and configuration, and the refractory period observed in the responses on single medullated nerve fibers. Am. J. Physiol. 134:1941;694-704.
55. Smith R.L., Clayton G.H., Wilcox C.L., Escudero K.W., Staley K.J. Differential expression of an inwardly rectifying chloride conductance in rat brain neurons. a potential mechanism for cell-specific modulation of postsynaptic inhibition J. Neurosci. 15:1995;4057-4067.
56. Staley K.J., Mody I. Shunting of excitatory input to dentate gyrus granule cells by a depolarizing GABAA receptor-mediated postsynaptic conductance. J. Neurophysiol. 68:1992;197-212.
57. Strange K., Singer T.D., Morrison R., Delpire E. Dependence of KCC2 K-Cl cotransporter activity on a conserved carboxy terminus tyrosine residue. Am. J. Physiol. Cell Physiol. 279:2000;C860-C867.
58. Stuart G., Spruston N., Sakmann B., Hausser M. Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci. 20:1997;125-131.
59. Sun D., Murali S.G. Na+-K+-2Cl- cotransporter in immature cortical neurons. A role in intracellular Cl- regulation J. Neurophysiol. 81:1999;1939-1948.
60. Takeya M., Hasuo H., Akasu T. Effects of temperature increase on the propagation of presynaptic action potentials in the pathway between the Schaffer collaterals and Hippocampal CA1 neurons. Neurosci. Res. 42:2002;175-185.
61. Thompson S.M., Gahwiler B.H. Activity-dependent disinhibition. I. Repetitive stimulation reduces IPSP driving force and conductance in the hippocampus in vitro. J. Neurophysiol. 61:1989;501-511. a.
62. Thompson S.M., Gahwiler B.H. Activity-dependent disinhibition. II. Effects of extracellular potassium, furosemide, and membrane potential on ECl- in hippocampal CA3 neurons. J. Neurophysiol. 61:1989;512-523. b.
63. Vardi N., Zhang L.L., Payne J.A., Sterling P. Evidence that different cation chloride cotransporters in retinal neurons allow opposite responses to GABA. J. Neurosci. 20:2000;7657-7663.
64. Vu T.Q., Payne J.A., Copenhagen D.R. Localization and developmental expression patterns of the neuronal K-Cl cotransporter (KCC2) in the rat retina. J. Neurosci. 20:2000;1414-1423.
65. Zhang L.I., Tao H.W., Holt C.E., Harris W.A., Poo M. A critical window for cooperation and competition among developing retinotectal synapses. Nature. 395:1998;37-44.
66. Zhou Q., Tao H.W., Poo M.M. Reversal and stabilization of synaptic modifications in developing visual system. Science. 20:2003;1953-1957.