Incorporation of inwardly rectifying AMPA receptors at silent synapses during hippocampal long-term potentiation

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1633, 2014, Pages

  Morita, Daiju ^a,b   Rah, Jong Cheol ^a,c   Isaac, John T R ^a,d  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b L Oréal Research Innovation   (Japan)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d ELI LILLY AND COMPANY   (United States)

Author keywords

Glutamate; Hippocampus; Synaptic plasticity

Indexed keywords

BRAIN; CALCIUM; ENZYME ACTIVITY; NEUROLOGY;

AMPA RECEPTOR; CALCIUM; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 2; GLUTAMIC ACID;

ANIMAL; ARTICLE; CYTOLOGY; ELECTROSTIMULATION; HIPPOCAMPUS; LONG TERM POTENTIATION; METABOLISM; NERVE CELL PLASTICITY; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; RAT; SYNAPSE;

GLUTAMATE; HIPPOCAMPUS; SYNAPTIC PLASTICITY;

ANIMALS; CALCIUM; ELECTRIC STIMULATION; HIPPOCAMPUS; LONG-TERM POTENTIATION; PATCH-CLAMP TECHNIQUES; RATS; RECEPTORS, AMPA; SYNAPSES;

EID: 84888785461     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2013.0156     Document Type: Article

References (38)

1. Malenka RC, Bear MF. 2004 LTP and LTD: an embarrassment of riches. Neuron 44, 5-21. (doi:10.1016/j.neuron.2004.09.012)
2. Bliss TV, Collingridge GL. 1993 A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39. (doi:10.1038/ 361031a0)
3. Malinow R, Malenka RC. 2002 AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25, 103-126. (doi:10.1146/annurev. neuro.25.112701.142758)
4. Collingridge GL, Isaac JT, Wang YT. 2004 Receptor trafficking and synaptic plasticity. Nat. Rev. Neurosci. 5, 952-962. (doi:10.1038/nrn1556)
5. Isaac JT, Nicoll RA, Malenka RC. 1995 Evidence for silent synapses: implications for the expression of LTP. Neuron 15, 427-434. (doi:10.1016/0896-6273(95)90046-2)
6. Isaac JT. 2003 Postsynaptic silent synapses: evidence and mechanisms. Neuropharmacology 45, 450-460. (doi:10.1016/S0028-3908(03)00229-6)
7. Kerchner GA, Nicoll RA. 2008 Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat. Rev. Neurosci. 9, 813-825. (doi:10.1038/ nrn2501)
8. Liao D, Hessler NA, Malinow R. 1995 Activation of postsynaptically silent synapses during pairinginduced LTP in CA1 region of hippocampal slice. Nature 375, 400-404. (doi:10.1038/375400a0)
9. Kullmann DM. 1994 Amplitude fluctuations of dual-component EPSCs in hippocampal pyramidal cells: implications for long-term potentiation. Neuron 12, 1111-1120. (doi:10.1016/0896-6273 (94)90318-2)
10. Durand GM, Kovalchuk Y, Konnerth A. 1996 Longterm potentiation and functional synapse induction in developing hippocampus. Nature 381, 71-75. (doi:10.1038/381071a0)
11. Hanse E, Durand GM, Garaschuk O, Konnerth A. 1997 Activity-dependent wiring of the developing hippocampal neuronal circuit. Semin. Cell Dev. Biol. 8, 35-42. (doi:10.1006/scdb.1996.0119)
12. Wu G, Malinow R, Cline HT. 1996 Maturation of a central glutamatergic synapse. Science 274, 972-976. (doi:10.1126/science.274.5289.972)
13. Ashby MC, Isaac JT. 2011 Maturation of a recurrent excitatory neocortical circuit by experiencedependent unsilencing of newly formed dendritic spines. Neuron 70, 510-521. (doi:10.1016/j.neuron. 2011.02.057)
14. Isaac JT, Crair MC, Nicoll RA, Malenka RC. 1997 Silent synapses during development of thalamocortical inputs. Neuron 18, 269-280. (doi:10.1016/S0896-6273(00)80267-6)
15. Busetto G, Higley MJ, Sabatini BL. 2008 Developmental presence and disappearance of postsynaptically silent synapses on dendritic spines of rat layer 2/3 pyramidal neurons. J. Physiol. 586, 1519-1527. (doi:10.1113/jphysiol. 2007.149336)
16. Daw MI, Scott HL, Isaac JT. 2007 Developmental synaptic plasticity at the thalamocortical input to barrel cortex: mechanisms and roles. Mol. Cell Neurosci. 34, 493-502. (doi:10.1016/j.mcn.2007.01.001)
17. Dingledine R, Borges K, Bowie D, Traynelis SF. 1999 The glutamate receptor ion channels. Pharmacol. Rev. 51, 7-61.
18. Isaac JT, Ashby MC, McBain CJ. 2007 The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 54, 859-871. (doi:10. 1016/j.neuron.2007.06.001)
19. 2+-permeable AMPA receptors in synaptic plasticity and neuronal death. Trends Neurosci. 30, 126-134. (doi:10.1016/j.tins. 2007.01.006)
20. Liu SJ, Cull-Candy SG. 2002 Activity-dependent change in AMPA receptor properties in cerebellar stellate cells. J. Neurosci. 22, 3881-3889.
21. Liu SQ, Cull-Candy SG. 2000 Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype. Nature 405, 454-458. (doi:10.1038/35013064)
22. Gardner SM, Takamiya K, Xia J, Suh JG, Johnson R, Yu S, Huganir RL. 2005 Calcium-permeable AMPA receptor plasticity is mediated by subunit-specific interactions with PICK1 and NSF. Neuron 45, 903-915. (doi:10.1016/j.neuron.2005.02.026)
23. 2+permeability of AMPARs at cerebellar synapses. Nat. Neurosci. 8, 768-775. (doi:10.1038/nn1468)
24. Plant K, Pelkey KA, Bortolotto ZA, Morita D, Terashima A, McBain CJ, Collingridge GL, Isaac JT. 2006 Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nat. Neurosci. 9, 602-604. (doi:10. 1038/nn1678)
25. Shepherd JD. 2012 Memory, plasticity and sleep: a role for calcium permeable AMPA receptors? Front. Mol. Neurosci. 5, 49. (doi:10.3389/fnmol. 2012.00049)
26. Man HY. 2011 GluA2-lacking, calcium-permeable AMPA receptors-inducers of plasticity? Curr. Opin. Neurobiol. 21, 291-298. (doi:10.1016/j.conb. 2011.01.001)
27. Tukey DS et al. 2013 Sucrose ingestion induces rapid AMPA receptor trafficking. J. Neurosci. 33, 6123-6132. (doi:10.1523/JNEUROSCI.4806-12.2013)
28. Hong I, Kim J, Kim J, Lee S, Ko HG, Nader K, Kaang BK, Tsien RW, Choi S. 2013 AMPA receptor exchange underlies transient memory destabilization on retrieval. Proc. Natl Acad. Sci. USA 110, 8218-8223.
29. Adesnik H, Nicoll RA. 2007 Conservation of glutamate receptor 2-containing AMPA receptors during long-term potentiation. J. Neurosci. 27, 4598-4602. (doi:10.1523/JNEUROSCI.0325-07.2007)
30. Gray EE, Fink AE, Sarinana J, Vissel B, O'Dell TJ. 2007 Long-term potentiation in the hippocampal CA1 region does not require insertion and activation of GluR2-lacking AMPA receptors. J. Neurophysiol. 98, 2488-2492. (doi:10.1152/jn.00473.2007)
31. Guire ES, Oh MC, Soderling TR, Derkach VA. 2008 Recruitment of calcium-permeable AMPA receptors during synaptic potentiation is regulated by CaM-kinase I. J. Neurosci. 28, 6000-6009. (doi:10. 1523/JNEUROSCI.0384-08.2008)
32. Lu Y, Allen M, Halt AR, Weisenhaus M, Dallapiazza RF, Hall DD, Usachev YM, McKnight GS, Hell JW. 2007 Age-dependent requirement of AKAP150-anchored PKA and GluR2-lacking AMPA receptors in LTP. EMBO J. 26, 4879-4890. (doi:10.1038/sj. emboj.7601884)
33. Sah P, Clements JD. 1999 Photolytic manipulation of [Ca2+]i reveals slow kinetics of potassium channels underlying the afterhyperpolarization in hippocampal pyramidal neurons. J. Neurosci. 19, 3657-3664.
34. 2+and short-term synaptic plasticity. Nature 371, 603-606. (doi:10.1038/371603a0)
35. Lu W, Shi Y, Jackson AC, Bjorgan K, During MJ, Sprengel R, Seeburg PH, Nicoll RA. 2009 Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron 62, 254-268. (doi:10.1016/j.neuron.2009.02.027)
36. 2+from separate presynaptic and postsynaptic intracellular stores. J. Neurosci. 16, 5951-5960.
37. Malenka RC, Lancaster B, Zucker RS. 1992 Temporal limits on the rise in postsynaptic calcium required for the induction of long-term potentiation. Neuron 9, 121-128. (doi:10.1016/ 0896-6273(92)90227-5)
38. Terashima A, Pelkey KA, Rah JC, Suh YH, Roche KW, Collingridge GL, McBain CJ, Isaac JT. 2008 An essential role for PICK1 in NMDA receptordependent bidirectional synaptic plasticity. Neuron 57, 872-882. (doi:10.1016/j.neuron.2008.01.028)