Conversion of silent synapses into the active pool by selective GluR1-3 and GluR4 AMPAR trafficking during in vitro classical conditioning

Journal of Neurophysiology

Volumn 98, Issue 3, 2007, Pages 1278-1286

  Mokin, Maxim ^a   Zheng, Zhaoqing ^a   Keifer, Joyce ^a  

^a UNIVERSITY OF SOUTH DAKOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; GLUTAMATE RECEPTOR 3; GLUTAMATE RECEPTOR 4; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RECEPTOR SUBUNIT; SYNAPTOPHYSIN;

ANIMAL TISSUE; ARTICLE; CELL FRACTIONATION; CONDITIONED REFLEX; CONDITIONING; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EYELID REFLEX; IMMUNOFLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; STATE DEPENDENT LEARNING; SYNAPSE;

ANIMALS; ASSOCIATION LEARNING; CONDITIONING, CLASSICAL; FEAR; MOTOR NEURONS; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTIC TRANSMISSION; TURTLES;

EID: 34548767661     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00212.2007     Document Type: Article

References (48)

1. Anderson CW, Keifer J. Properties of conditioned abducens nerve responses in a highly reduced in vitro brain stem preparation from the turtle. J Neurophysiol 81: 1242-1250, 1999.
2. Antonova I, Arancio O, Trillat AC, Wang HG, Zablow L, Udo H, Kandel ER, Hawkins RD. Rapid increase in clusters of presynaptic proteins at onset of long-lasting potentiation. Science 294: 1457-1550, 2001.
3. Ashby MC, Maier SR, Nishimune A, Henley JM. Lateral diffusion drives constitutive exchange of AMPA receptors at dendritic spines and is regulated by spine morphology. J Neurosci 26: 7046-7055, 2006.
4. Attwell PJ, Rahman S, Ivarsson M, Yeo CH. Cerebellar cortical AMPA-kainate receptor blockade prevents performance of classically conditioned nictitating membrane responses. J Neurosci 19: RC45, 1999.
5. Bramham CR, Messaoudi E. BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis. Progress Neurobiol 76: 99-125, 2006.
6. Collingridge GL, Isaac JTR, Wang YT. Receptor trafficking and synaptic plasticity. Nat Neurosci 5: 952-962, 2002.
7. Dunkley PR, Heath JW, Harrison SM, Jarvie PE, Glenfield PJ, Rostas JA. A rapid Percoll gradient procedure for isolation of synaptosomes directly from an S1 fraction: homogeneity and morphology of subcellular fractions. Brain Res 441: 59-71, 1988.
8. Gasparini S, Saviane C, Voronin LL, Charubini E. Silent synapses in the developing hippocampus: lack of functional AMPA receptors or low probability of glutamate release? Proc Natl Acad Sci USA 97: 9741-9746, 2000.
9. Geinisman Y, Berry RW, Disterhoft JF, Power JM, Van der Zee EA. Associative learning elicits the formation of multiple-synapse boutons. J Neurosci 21: 5568-5573, 2001.
10. Gomperts SN, Rao A, Craig AM, Malenka RC, Nicoll RA. Postsynaptically silent synapses in single neuron cultures. Neuron 21: 1443-1451, 1998.
11. Groc L, Gustafsson B, Hanse E. AMPA signalling in nasent glutamatergic synapses: there and not there! Trends Neurosci 29: 132-139, 2006.
12. Grosshans DR, Clayton DA, Coultrap SJ, Browning MD. LTP leads to rapid surface expression of NMDA but not AMPA receptors in adult rat CA1. Nat Neurosci 5: 27-33, 2002.
13. Isaac JT, Nicoll RA, Malenka RC. Evidence for silent synapses: implications for the expression of LTP. Neuron 15: 427-434, 1995.
14. Keifer J. In vitro eye-blink reflex model: role of excitatory amino acids and labeling of network activity with sulforhodamine. Exp Brain Res 97: 239-253, 1993.
15. Keifer J. In vitro eye-blink classical conditioning is NMDA receptor-dependent and involves redistribution of AMPA receptor subunit GluR4. J Neurosci 21: 2434-2441, 2001.
16. Keifer J. In vitro classical conditioning of the turtle eyeblink reflex: approaching cellular mechanisms of acquisition. Cerebellum 2: 55-61, 2003.
17. Keifer J, Armstrong KE, Houk JC. In vitro classical conditioning of abducens nerve discharge in turtles. J Neurosci 15: 5036-5048, 1995.
18. Keifer J, Carr MT. Immunocytochemical localization of glutamate receptor subunits in the brain stem and cerebellum of the turtle Chrysemys picta. J Comp Neurol 427: 455-468, 2000.
19. Keifer J, Clark TG. Abducens conditioning in in vitro turtle brain stem without cerebellum requires NMDA receptors and involves upregulation of GluR4-containing AMPA receptors. Exp Brain Res 151: 405-410, 2003.
20. Keifer J, Mokin M. Distribution of anterogradely labeled trigeminal and auditory nerve boutons on abducens motor neurons in turtles: implications for in vitro classical conditioning. J Comp Neurol 471: 144-152, 2004.
21. Keifer J, Zheng Z-Q, Zhu D. MAPK signalling pathways mediate AMPA receptor trafficking in an in vitro model of classical conditioning. J Neurophyiol 97: 2067-2074, 2007.
22. Kim JH, Udo H, Li HL, Youn TY, Chen M, Kandel ER, Bailey CH. Presynaptic activation of silent synapses and growth of new synapses contribute to intermediate and long-term facilitation in Aplysia. Neuron 40: 151-165, 2003.
23. Kleim JA, Freeman JH, Bruneau R, Nolan BC, Cooper NR, Zook A, Walters D. Synapse formation is associated with memory storage in the cerebellum. Proc Natl Acad Sci USA 99: 13228-13231, 2002.
24. Kullmann DM. Amplitude fluctuations of dual-component EPSCs in hippocampal pyramidal cells: implications for long-term potentiation. Neuron 12: 1111-1120, 1994.
25. Liao D, Hessler NA, Malinow R. Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375: 400-404, 1995.
26. Liao D, Zhang X, O'Brian R, Ehlers MD, Huganir RL. Regulation of morphological postsynaptic silent synapses in developing hippocampal neurons. Nat Neurosci 2: 37-43, 1999.
27. Lissin DV, Carroll RC, Nicoll RA, Malenka RC, von Zastrow M. Rapid, activation-induced redistribution of ionotropic glutamate receptors in cultured hippocampal neurons. J Neurosci 19: 1263-1272, 1999.
28. Malinow R, Malenka RC. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25: 103-126, 2002.
29. Maren S, Quirk GJ. Neuronal signalling of fear memory. Nat Rev Neurosci 5: 844-852, 2004.
30. Miserendino MJ, Sananes CB, Melia FR, Davis M. Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala. Nature 345: 716-718, 1990.
31. Mokin M, Keifer J. Targeting of GluR4-containing AMPA receptors to synaptic sites during in vitro classical conditioning. Neuroscience 128: 219-228, 2004.
32. Mokin M, Keifer J. Quantitative analysis of immunofluorescent punctate staining of synaptically localized proteins using confocal microscopy and stereology. J Neurosci Methods 157: 218-224, 2006.
33. Mokin M, Lindahl JS, Keifer J. Immediate-early gene-encoded protein Arc is associated with synaptic delivery of GluR4-containing AMPA receptors during in vitro classical conditioning. J Neurophysiol 95: 215-224, 2006.
34. Moyer JR, Thompson LT, Disterhoft JF. Trace eyeblink conditioning increases CA1 excitability in a transient and learning-specific manner. J Neurosci 16: 5536-5546, 1996.
35. Nusser Z, Lujan R, Laube G, Roberts JD, Molnar E, Somogyi P. Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21: 545-559, 1998.
36. Petralia RS, Esteban JA, Wang YX, Partridge JG, Zhao HM, Wenthold RJ, Malinow R. Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses. Nat Neurosci 2: 31-36, 1999.
37. Racca C, Stephenson FA, Streit P, Roberts JD, Somogyi P. NMDA receptor content of synapses in stratum radiatum of the hippocampal CA1 area. J Neurosci 20: 2512-2522, 2000.
38. Reid CA, Dixon DB, Takahashi M, Bliss TV, Fine A. Optical quantal analysis indicates that long-term potentiation at single hippocampal mossy fiber synapses is expressed through increased release probability, recruitment of new release sites, and activation of silent synapses. J Neurosci 24: 3618-3626, 2004.
39. 2+/calmodulin-dependent protein kinase II at lateral amygdala synapses. J Neurosci 24: 3281-3288, 2004.
40. Rodrigues SM, Schafe GE, LeDoux JE. Intra-amygdala blockade of the NR2B subunit of the NMDA receptor disrupts the acquisition but not the expression of fear conditioning. J Neurosci 21: 6889-6896, 2001.
41. Rumpel S, LeDoux J, Zador A, Malinow R. Postsynaptic receptor trafficking underlying a form of associative learning. Science 308: 83-88, 2005.
42. Schafe GE, Atkins CM, Swank MW, Bauer EP, Sweatt JD, LeDoux JE. Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of Pavlovian fear conditioning. J Neurosci 20: 8177-8187, 2000.
43. Servatius RJ, Shors TJ. Early acquisition, but not not retention, of the classically conditioned eyeblink esponse is N-methyl-D-aspartate (NMDA) receptor dependent. Behav Neurosci 110: 1040-1048, 1996.
44. Shi S-H, Hayashi Y, Petralia RS, Zaman SH, Wenthold RJ, Svoboda K, Malinow R. Rapid spine delivery and redistribution of AMPA receptors and synaptic NMDA receptor activation. Science 299: 1585-1588, 1999.
45. Takumi Y, Ramirez-Leon V, Laake P, Rinvik E, Ottersen OP. Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat Neurosci 2: 618-624, 1999.
46. Tocco G, Devgan KK, Hauge SA, Weiss C, Baudry M, Thompson RF. Classical conditioning selectively increases AMPA receptor binding in rabbit hippocampus. Brain Res 559: 331-336, 1991.
47. Yeh SH, Mao SC, Lin HC, Gean PW. Synaptic expression of glutamate receptors after encoding of fear memory in the rat amygdala. Mol Pharmacol 69: 299-308, 2006.
48. Zhen X, Du W, Romano AG, Friedman E, Harvey JA. The p38 mitogenactivated protein kinase is involved in associative learning in rabbits. J Neurosci 21: 5513-5519, 2001.