Distinct roles for ionotropic and metabotropic glutamate receptors in the maturation of excitatory synapses

Journal of Neuroscience

Volumn 20, Issue 6, 2000, Pages 2229-2237

  Gomperts, Stephen N ^a   Carroll, Reed ^b,c   Malenka, Robert C ^b,c   Nicoll, Roger A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Autapse; Development; Glutamate receptors; Ionotropic; Metabotropic; Silent synapse

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR ANTAGONIST; IONOTROPIC RECEPTOR; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; SODIUM CHANNEL; TETRODOTOXIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR DENSITY; SYNAPTOGENESIS;

EID: 0034653962     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-06-02229.2000     Document Type: Article

References (49)

1. Allen CN, Brady R, Swann J, Hori N, Carpenter DO (1988) N-Methyl-D-aspartate (NMDA) receptors are inactivated by trypsin. Brain Res 458:147-150.
2. Allison DW, Gelfand VI, Spector I, Craig AM (1998) Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: differential attachment of NMDA versus AMPA receptors. J Neurosci 18:2423-2436.
3. Basarsky TA, Parpura V, Haydon PG (1994) Hippocampal synaptogenesis in cell culture: developmental time course of synapse formation, calcium influx, and synaptic protein distribution. J Neurosci 14:6402-6411.
4. Bekkers JM, Stevens CF (1989) NMDA and non-NMDA receptors are co-localized at individual excitatory synapses in cultured rat hippocampus. Nature 341:230-233.
5. Benson DL, Cohen PA (1996) Activity-independent segregation of excitatory and inhibitory synaptic terminals in cultured hippocampal neurons. J Neurosci 16:64246432.
6. Cohen MW (1972) The development of neuromuscular connexions in the presence of D-tubocurarine. Brain Res 41:457-463.
7. 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.
8. Craig AM, Blackstone CD, Huganir RL, Banker G (1993) The distribution of glutamate receptors in cultured rat hippocampal neurons: postsynaptic clustering of AMPA-selective subunits. Neuron 10:1055-1068.
9. Craig AM, Blackstone CD, Huganir RL, Banker G (1994) Selective clustering of glutamate and gamma-aminobutyric acid receptors opposite terminals releasing the corresponding neurotransmitters. Proc Natl Acad Sci USA 91:12373-12377.
10. Davey DF, Cohen MW (1986) Localization of acetylcholine receptors and cholinesterase on nerve-contacted and noncontacted muscle cells grown in the presence of agents that block action potentials. J Neurosci 6:673-680.
11. Durand GM, Kovalchuk Y, Konnerth A (1996) Long-term potentiation and functional synapse induction in developing hippocampus. Nature 381:71-75.
12. Gomperts SN (1996) Clustering membrane proteins: it's all coming together with the PSD-95/SAP90 protein family. Cell 84:659-662.
13. Gomperts SN, Rao A, Craig AM, Malenka RC, Nicoll RA (1998) Postsynaptically silent synapses in single neuron cultures. Neuron 21:1443-1451.
14. Hsia A, Malenka RC, Nicoll RA (1998) Development of excitatory circuitry in the hippocampus. J Neurophysiol 79:2013-2024.
15. Hsueh YP, Sheng M (1998) Anchoring of glutamate receptors at the synapse. Prog Brain Res 116:123-131.
16. Isaac JTR, Nicoll RA, Malenka RC (1995) Evidence for silent synapses: implications for the expression of LTP. Neuron 15:427-434.
17. Isaac JTR, Crair MC, Nicoll RA, Malenka RC (1997) Silent synapses during development of thalamocortical inputs. Neuron 18:269-280.
18. Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
19. Kimura F, Otsu Y, Tsumoto T (1997) Presynaptically silent synapses: spontaneously active terminals without stimulus-evoked release demonstrated in cortical autapses. J Neurophysiol 77:2805-2815.
20. Kirsch J, Betz H (1998) Glycine-rcceptor activation is required for receptor clustering in spinal neurons. Nature 392:717-720.
21. Kiyosue K, Kasai M, Taguchi T (1996) Two modes of activity-dependent synaptogenesis of cerebral neurons in vitro. NeuroReport 7:701-704.
22. Kossel AH, Williams CV, Schweizer M, Kater SB (1997) Afferent innervation influences the development of dendritic branches and spines via both activity-dependent and nonactivity-dependent mechanisms. J Neurosci 17:6314-6324.
23. Lerma J, Morales M, Vicente MA, Herreras O (1997) Glutamate receptors of the kainate type and synaptic transmission. Trends Neurosci 20:9-12.
24. 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.
25. Liao D, Zhang X, O'Brien R, Ehlers MD, Huganir RL (1999) Regulation of morphological postsynaptic silent synapses in developing hippocampal neurons. Nat Neurosci 2:37-43.
26. Liu G, Tsien RW (1495) Properties of synaptic transmission at single hippocampal synaptic boutons. Nature 375:404-408.
27. Lu YM, Jia Z, Janus C, Henderson JT, Gerlai R, Wojtowicz JM, Roder JC (1997) Mice lacking metabotropic glutamate receptor 5 show impaired learning and reduced CA1 long-term potentiation (LTP) but normal CA3 LTP. J Neurosci 17:5196-5205.
28. Mammen AL, Huganir RL, O'Brien RJ (1997) Redistribution and stabilization of cell surface glutamate receptors during synapse formation. J Neurosci 17:7351-7358.
29. Manabe T, Wyllie DJA, 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.
30. McKinney RA, Capogna M, Durr R, Gahwiler BH, Thompson SM (1999) Miniature synaptic events maintain dendritic spines via AMPA receptor activation. Nat Neurosci 2:44-49.
31. Murase K, Ryu PD, Randic M (1989) Excitatory and inhibitory amino acids and peptide-induced responses in acutely isolated rat spinal dorsal horn neurons. Neurosci Lett 103:56-63.
32. Nguyen QT, Lichtman JW (1996) Mechanism of synapse disassembly at the developing neuromuscular junction. Curr Opin Neurobiol 6:104-112.
33. Nusser Z, Lujan R, Laube G, Roberts JDB, Molar E, Somogyi P (1998) Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21:545-559.
34. O'Brien RJ, Mammen AL, Blackshaw S, Ehlers MD, Rothstein JD, Huganir RL (1997) The development of excitatory synapses in cultured spinal neurons. J Neurosci 17:7339-7350.
35. O'Brien RJ, Lau LF, Huganir RL (1998) Molecular mechanisms of glutamate receptor clustering at excitatory synapses. Curr Opin Neurobiol 8:364-369.
36. O'Brien RJ, Xu D, Petralia RS, Steward O, Huganir RL, Worley P (1999) Synaptic clustering of AMPA receptors by the extracellular immediate-early gene product NARP. Neuron 23:309-323.
37. Oliet SHR, Malenka RC, Nicoll RA (1997) Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neuron 18:969-982.
38. Petralia RS, Esteban JA, Wang YX, Partridge JG, Zhao HM, Wenthold RJ, Malinow R (1999) Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses. Nat Neurosci 2:31-36.
39. Rao A, Craig AM (1997) Activity regulates the synaptic localization of the NMDA receptor in hippocampal neurons. Neuron 19:801-812.
40. Rao A, Kim E, Sheng M, Craig AM (1998) Heterogeneity in the molecular composition of excitatory postsynaptic sites during development of hippocampal neurons in culture. J Neurosci 18:1217-1229.
41. Rumpel S, Hatt H, Gottmann K (1998) Silent synapses in the developing rat visual cortex: evidence for postsynaptic expression of synaptic plasticity. J Neurosci 18:8863-8874.
42. Rutherford LC, Nelson SB, Turrigiano GG (1998) BDNF has opposite effects on the quantal amplitude of pyramidal neuron and interneuron excitatory synapses. Neuron 21:521-530.
43. Segal MM, Furshpan EJ (1990) Epileptiform activity in microcultures containing small numbers of hippocampal neurons. J Neurophysiol 64:1390-1399.
44. Silva AJ, Stevens CF, Tonegawa S, Wang Y (1992) Deficient hippocampal long-term potentiation in alpha calcium-calmodulin kinase II mutant mice. Science 257:201-206.
45. Steward O, Falk PM (1991) Selective localization of polyribosomes beneath developing synapses: a quantitative analysis of the relationships between polyribosomes and developing synapses in the hippocampus and dentate gyrus. J Comp Neurol 314:545-557.
46. Takumi Y, Ramirez-Leon V, Laake P, Rinvik E, Ottersen OP (1999) Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat Neurosci 2:618-624.
47. Tong G, Jahr CE (1994) Block of glutamate transporters potentiates postsynaptic excitation. Neuron 13:1195-1203.
48. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391:892-896.
49. Wu G, Malinow R, Cline HT (1996) Maturation of a central glutamatergic synapse. Science 274:972-976.