Mechanisms of induction and expression of long-term depression at GABAergic synapses in the neonatal rat hippocampus

Journal of Neuroscience

Volumn 19, Issue 17, 1999, Pages 7568-7577

  Caillard, Olivier ^a,b   Ben Ari, Yehezkel ^a   Gaïarsa, Jean Luc ^a  

^a INSERM   (France)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

Calcium; Development; GABA; Glutamate; Hippocampus; Synaptic plasticity

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; GLUTAMIC ACID; MAGNESIUM ION; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POSTSYNAPTIC RECEPTOR; PRESYNAPTIC RECEPTOR; STRONTIUM;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GABAERGIC SYSTEM; HIPPOCAMPUS; MALE; MEMBRANE DEPOLARIZATION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEWBORN; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; QUANTUM THEORY; RAT; SYNAPTOGENESIS;

EID: 0033198169     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-17-07568.1999     Document Type: Article

References (46)

1. Alger BE, Pitler TA, Wagner JJ, Martin LA, Morishita W, Kirov SA, Lenz RA (1996) Retrograde signalling in depolarization-induced suppression of inhibition in rat hippocampal CA1 cells. J Physiol (Lond) 496:197-209.
2. Amaral DG, Dent JA (1981) Development of the mossy fibers of the dentate gyrus: light and electron microscopic study of the mossy fibers and their expansions. J Comp Neurol 195:51-86.
3. Bear MF, Malenka RC (1994) Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol 4:389-399.
4. Ben-Ari Y, Represa A (1990) Brief seizure episodes induce long-term potentiation and mossy fibre sprouting in the hippocampus. Trends Neurosci 13:312-318.
5. Ben-Ari Y, Cherubini E, Corradetti R, Gaïarsa J-L (1989) Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol (Lond) 416:303-325.
6. A, NMDA and AMPA receptors: a developmentally regulated "ménage a trois." Trends Neurosci 20:523-529.
7. Caillard O, Ben-Ari Y, Gaïarsa J-L (1999) Long-term potentiation of GABAergic synaptic transmission in neonatal rat hippocampus J Physiol (Lond) 518:109-119.
8. Charpier S, Behrends JC, Triller A, Faber DS, Korn H (1995) "Latent" inhibitory connections become functional during activity-dependent plasticity. Proc Natl Acad Sci USA 92:117-120.
9. Constantine-Paton M, Cline HT (1998) LTP and activity dependent synaptogenesis: the more alike they are, the more different they become. Curr Opin Neurobiol 8:139-148.
10. Crepel V, Hammond C, Krnjevic K, Chinestra P, Ben-Ari Y (1993) Anoxia-induced LTP of isolated NMDA receptor-mediated synaptic responses. J Neurophysiol 69:1774-1778.
11. Faber DS, Korn H (1991) Applicability of the coefficient of variation method for analysing synaptic plasticity. Biophys J 60:1288-1294.
12. Fitzsimonds RM, Poo MM (1998) Retrograde signalling in the development and modification of synapses. Physiol Rev 78:143-170.
13. Glitsch M, Llano I, Marty A (1996) Glutamate as a candidate retrograde messenger at interneurone-Purkinje cell synapses of rat cerebellum. J Physiol (Lond) 497:531-537.
14. Goodman CS, Shatz CJ (1993) Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72:77-98.
15. Isaac JTR, Nicoll RA, Malenka RC (1995) Evidence for silent synapses: implications for the expression of LTP. Neuron 15:427-434.
16. Isaac JTR, Crair MC, Nicoll RA, Malenka RC (1997) Silent synapses during development of thalamocortical inputs. Neuron 18:269-280.
17. Kano M (1996) Long-lasting potentiation of GABAergic inhibitory synaptic transmission in cerebellar Purkinje cells: its properties and possible mechanisms. Behav Brain Sci 19:354-364.
18. Kano M, Rexhausen U, Dreessen J, Konnerth A (1992) Synaptic excitation produces a long-lasting rebound potentiation of inhibitory synaptic signals in cerebellar Purkinje cells. Nature 356:601-604.
19. Khazipov R, Leinekugel X, Khalilov I, Gaïarsa J-L, Ben-Ari Y (1997) Synchronization of GABAergic interneuronal network in CA3 subfield of neonatal rat hippocampal slices. J Physiol (Lond) 498:763-772.
20. 2+ release are involved in the induction of long-term potentiation at visual cortical inhibitory synapses. J Neurosci 16:6342-6352.
21. Komatsu Y, Iwakiri M (1993) Long-term modification of inhibitory synaptic transmission in developing visual cortex. NeuroReport 4:907-910.
22. 2+ oscillations mediated by the synergistic excitatory actions of GABAA and NMDA receptors in the neonatal hippocampus. Neuron 18:243-255.
23. Liao D, Hessler NA, Malinow R (1995) Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375:400-404.
24. Llano I, Leresche N, Marty A (1991) Calcium entry increases the sensitivity of cerebellar Purkinje cells to applied GABA and decreases inhibitory synaptic currents. Neuron 6:565-574.
25. Manabe T, Nicoll RA (1994) Long-term potentiation: evidence against an increase in transmitter release probability in the CA1 region of the hippocampus. Science 265:1888-1892.
26. Manabe T, Wyllie DJ, Perkel DJ, Nicoll RA (1993) Modulation of synaptic transmission and long-term potentiation: effects on paired pulse facilitation and EPSC variance in the CA1 region of the hippocampus. J Neurophysiol 70:1451-1459.
27. A-mediated polysynaptic potentials in the neonatal rat hippocampal CA3 region. Eur J Neurosci 7:1442-1448.
28. McLean HA, Caillard O, Ben-Ari Y, Gaïarsa J-L (1996) Bidirectional plasticity expressed by GABAergic synapses in the neonatal rat hippocampus. J Physiol (Lond) 496:471-477.
29. Miledi R (1966) Strontium as a substitute for calcium in the process of transmitter release at the neuromuscular junction. Nature 212:1233-1234.
30. Mogul DJ, Fox AP (1991) Evidence for multiple types of Ca2+ channels in acutely isolated hippocampal CA3 neurones of the guinea-pig. J Physiol (Lond) 433:259-281.
31. Morishita W, Alger BE (1997) Sr2+ supports depolarization-induced suppression of inhibition and provides new evidence for a presynaptic expression mechanism in rat hippocampal slices. J Physiol (Lond) 505:307-317.
32. Morishita W, Sastry BR (1993) Long-term depression of IPSPs in rat deep cerebellar nuclei. NeuroReport 4:719-722.
33. Morishita W, Sastry BR (1996) Postsynaptic mechanisms underlying long-term depression of GABAergic transmission in neurons of the deep cerebellar nuclei. J Neurophysiol 76:59-68.
34. Morishita W, Kirov, SA, Alger BE (1998) Evidence for metabotropic glutamate receptor activation in the induction of depolarization-induced suppression of inhibition in hippocampal CA1. J Neurosci 18:4870-4882.
35. Nowak L, Bregestovski P, Ascher P, Herbet A, Prochiantz A (1984) Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307:462-465.
36. Nusser Z, Hajos N, Somogyi P, Mody I (1998) Increased number of synaptic GABA(A) receptors underlies potentiation at hippocampal inhibitory synapses. Nature 395:172-177.
37. Oda Y, Charpier S, Murayama Y, Suma C, Korn H (1995) Long-term potentiation of glycinergic inhibitory synaptic transmission. J Neurophysiol 74:1056-1074.
38. Oliet SHR, Malenka RC, Nicoll RA (1996) Bidirectional control of quantal size by synaptic activity in the hippocampus. Science 271:1294-1297.
39. Oliet SHR, Malenka RC, Nicoll RA (1997) Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neuron 18:969-982.
40. 2+ from separate presynaptic and postsynaptic intracellular stores. J Neurosci 16:5951-5960.
41. Rumpel E, Behrends JC (1999) Sr2+-dependent asynchronous evoked transmission of rat striatal inhibitory synapses in vitro. J Physiol (Lond) 514.2:447-458.
42. Stelzer A, Slater NT, ten Bruggencate G (1987) Activation of NMDA receptors blocks GABAergic inhibition in an in vitro model of epilepsy. Nature 326:698-701.
43. Super H, Soriano E (1994) The organisation of the embryonic and early postnatal murine hippocampus. II. Development of entorhinal, commissural and septal connections studied with the lipophilic tracer DiI. J Comp Neurol 344:101-120.
44. Thompson SM, Gähwiler BH (1992) Comparison of the actions of baclofen at pre- and postsynaptic receptors in the rat hippocampus in vitro. J Physiol (Lond) 451:329-345.
45. Thompson SM, Wong RKS (1991) Development of calcium current subtypes in isolated rat hippocampal pyramidal cells. J Physiol (Lond) 439:671-689.
46. Wang JH, Stelzer A (1996) Shared calcium signalling pathways in the induction of long-term potentiation and synaptic disinhibition in CA1 pyramidal cell dendrites. J Neurophysiol 75:1687-1702.