Impaired associative fear learning in mice with complete loss or haploinsufficiency of AMPA GluR1 receptors

Frontiers in Behavioral Neuroscience

Volumn 1, Issue DEC, 2007, Pages

  Feyder, Michael ^a   Wiedholz, Lisa ^a   Sprengel, Rolf ^b   Holmes, Andrew ^a  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^b MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

Author keywords

AMPA; GluR1; Glutamate; Learning; Mouse

Indexed keywords

EID: 84901985938     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/neuro.08.004.200710.3389/neuro.08.004.2007     Document Type: Article

References (51)

1. Balleine, B. W., and Dickinson, A. (1998). Goal-directed instrumental action: contingency and incentive learning and their cortical substrates. Neuropharmacology 37, 407-419.
2. Bannerman, D. M., Deacon, R. M., Brady, S., Bruce, A., Sprengel, R., Seeburg, P. H., and Rawlins, J. N. (2004). A comparison of GluR-A-deficient and wild-type mice on a test battery assessing sensorimotor, affective, and cognitive behaviors. Behav. Neurosci. 118, 643-647.
3. Bannerman, D. M., Rawlins, J. N., and Good, M. A. (2006). The drugs don't work-or do they? Pharmacological and transgenic studies of the contribution of NMDA and GluRA-containing AMPA receptors to hippocampal-dependent memory. Psychopharmacology (Berl) 188, 552-566.
4. Bast, T., da Silva, B. M., and Morris, R. G. M. (2005). Distinct Contributions of Hippocampal NMDA and AMPA Receptors to Encoding and Retrieval of One-Trial Place Memory. J. Neurosci. 25, 5845-5856.
5. Bonini, J. S., Rodrigues, L., Kerr, D. S., Bevilaqua, L. R., Cammarota, M., and Izquierdo, I. (2003). AMPA/kainate and group-I metabotropic receptor antagonists infused into different brain areas impair memory formation of inhibitory avoidance in rats. Behav. Pharmacol. 14, 161-166.
6. Boyce-Rustay, J. M., and Holmes, A. (2006). Genetic inactivation of the NMDA receptor NR2A subunit has anxiolytic-and antidepressant-like effects in mice. Neuropsychopharmacology 31, 2405-2414.
7. Bozon, B., Davis, S., and Laroche, S. (2003). A requirement for the immediate early gene zif268 in reconsolidation of recognition memory after retrieval. Neuron 40, 695-701.
8. Collingridge, G. L., Isaac, J. T., and Wang, Y. T. (2004). Receptor trafficking and synaptic plasticity. Nat. Rev. Neurosci. 5, 952-962.
9. Cravens, C. J., Vargas-Pinto, N., Christian, K. M., and Nakazawa, K. (2006). CA3 NMDA receptors are crucial for rapid and automatic representation of context memory. Eur. J. Neurosci. 24, 1771-1780.
10. Day, M., Langston, R., and Morris, R. G. (2003). Glutamate-receptor-mediated encoding and retrieval of paired-associate learning. Nature 424, 205-209.
11. De Leonibus, E., Costantini, V. J., Castellano, C., Ferretti, V., Oliverio, A., and Mele, A. (2003). Distinct roles of the different ionotropic glutamate receptors within the nucleus accumbens in passive-avoidance learning and memory in mice. Eur. J. Neurosci. 18, 2365-2373.
12. Dere, E., Huston, J. P., and De Souza Silva, M. A. (2007). The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents. Neurosci. Biobehav. Rev. 31, 673-704.
13. Everitt, B., Cardinal, R., Hall, J., Parkinson, J., and Robbins, T. (2000). Differential involvement of amygdala subsystems in appetitive conditioning and drug addiction. In The amygdala, Vol. 2, J. Aggleton, ed. (New York, Oxford University Press), pp. 353-390.
14. Fanselow, M. S., and LeDoux, J. E. (1999). Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala. Neuron 23, 229-232.
15. Fanselow, M. S., and Poulos, A. M. (2005). The neuroscience of mammalian associative learning. Annu. Rev. Psychol. 56, 207-234.
16. Hartmann, B., Ahmadi, S., Heppenstall, P. A., Lewin, G. R., Schott, C., Borchardt, T., Seeburg, P. H., Zeilhofer, H. U., Sprengel, R., and Kuner, R. (2004). The AMPA receptor subunits GluR-A and GluR-B reciprocally modulate spinal synaptic plasticity and inflammatory pain. Neuron 44, 637-650.
17. Hatfield, T., Han, J. S., Conley, M., Gallagher, M., and Holland, P. (1996). Neurotoxic lesions of basolateral, but not central, amygdala interfere with Pavlovian secondorder conditioning and reinforcer devaluation effects. J. Neurosci. 16, 5256-5265.
18. Hefner, K., and Holmes, A. (2007). An investigation of the behavioral actions of ethanol across adolescence in mice. Psychopharmacology (Berl) 191, 311-322.
19. Hitchcott, P. K., and Phillips, G. D. (1997). Amygdala and hippocampus control dissociable aspects of drug-associated conditioned rewards. Psychopharmacology (Berl) 131, 187-195.
20. Hoffman, D. A., Sprengel, R., and Sakmann, B. (2002). Molecular dissection of hippocampal theta-burst pairing potentiation. Proc. Natl. Acad. Sci. USA 99, 7740-7745.
21. Hu, H., Real, E., Takamiya, K., Kang, M. G., Ledoux, J., Huganir, R. L., and Malinow, R. (2007). Emotion enhances learning via norepinephrine regulation of AMPA-receptor trafficking. Cell 131, 160-173.
22. Huerta, P. T., Sun, L. D., Wilson, M. A., and Tonegawa, S. (2000). Formation of temporal memory requires NMDA receptors within CA1 pyramidal neurons. Neuron 25, 473-480.
23. Humeau, Y., Reisel, D., Johnson, A. W., Borchardt, T., Jensen, V., Gebhardt, C., Bosch, V., Gass, P., Bannerman, D. M., Good, M. A., Hvalby, O., Sprengel, R., and Lüthi, A. (2007). A pathway-specific function for different AMPA receptor subunits in amygdala LTP and fear conditioning. J. Neurosci. 27, 10947-10956.
24. Johnson, A. W., Bannerman, D. M., Rawlins, N. P., Sprengel, R., and Good, M. A. (2005). Impaired outcome-specific devaluation of instrumental responding in mice with a targeted deletion of the AMPA receptor glutamate receptor 1 subunit. J. Neurosci. 25, 2359-2365.
25. Jones, M. W., Errington, M. L., French, P. J., Fine, A., Bliss, T. V., Garel, S., Charnay, P., Bozon, B., Laroche, S., and Davis, S. (2001). A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat. Neurosci. 4, 289-296.
26. Kim, J. J., and Fanselow, M. S. (1992). Modality-specific retrograde amnesia of fear. Science 256, 675-677.
27. Kim, J. J., Clark, R. E., and Thompson, R. F. (1995). Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. Behav. Neurosci. 109, 195-203.
28. Kogan, J. H., Frankland, P. W., Blendy, J. A., Coblentz, J., Marowitz, Z., Schutz, G., and Silva, A. J. (1997). Spaced training induces normal long-term memory in CREB mutant mice. Curr. Biol. 7, 1-11.
29. LeDoux, J. E. (2000). Emotion circuits in the brain. Annu. Rev. Neurosci. 23, 155-184.
30. Lledo, P. M., Zhang, X., Sudhof, T. C., Malenka, R. C., and Nicoll, R. A. (1998). Postsynaptic membrane fusion and long-term potentiation. Science 279, 399-403.
31. Mack, V., Burnashev, N., Kaiser, K. M., Rozov, A., Jensen, V., Hvalby, O., Seeburg, P. H., Sakmann, B., and Sprengel, R. (2001). Conditional restoration of hippocampal synaptic potentiation in Glur-A-deficient mice. Science 292, 2501-2504.
32. Malinow, R., and Malenka, R. C. (2002). AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25, 103-126.
33. Maren, S., and Quirk, G. J. (2004). Neuronal signalling of fear memory. Nat. Rev. Neurosci. 5, 844-852.
34. McDonald, A. J. (1996). Localization of AMPA glutamate receptor subunits in subpopulations of non-pyramidal neurons in the rat basolateral amygdala. Neurosci. Lett. 208, 175-178.
35. Mead, A. N., and Stephens, D. N. (2003). Selective disruption of stimulus-reward learning in glutamate receptor gria1 knock-out mice. J. Neurosci. 23, 1041-1048.
36. Mead, A. N., Brown, G., Le Merrer, J., and Stephens, D. N. (2005). Effects of deletion of gria1 or gria2 genes encoding glutamatergic AMPA-receptor subunits on place preference conditioning in mice. Psychopharmacology (Berl) 179, 164-171.
37. Misane, I., Tovote, P., Meyer, M., Spiess, J., Ogren, S. O., and Stiedl, O. (2005). Timedependent involvement of the dorsal hippocampus in trace fear conditioning in mice. Hippocampus 15, 418-426.
38. Nakazawa, K., Sun, L. D., Quirk, M. C., Rondi-Reig, L., Wilson, M. A., and Tonegawa, S. (2003). Hippocampal CA3 NMDA receptors are crucial for memory acquisition of one-time experience. Neuron 38, 305-315.
39. Reisel, D., Bannerman, D. M., Schmitt, W. B., Deacon, R. M., Flint, J., Borchardt, T., Seeburg, P. H., and Rawlins, J. N. (2002). Spatial memory dissociations in mice lacking GluR1. Nat. Neurosci. 5, 868-873.
40. Rumpel, S., LeDoux, J., Zador, A., and Malinow, R. (2005). Postsynaptic receptor trafficking underlying a form of associative learning. Science 308, 83-88.
41. Schmitt, W. B., Deacon, R. M., Seeburg, P. H., Rawlins, J. N., and Bannerman, D. M. (2003). A within-subjects, within-task demonstration of intact spatial reference memory and impaired spatial working memory in glutamate receptor-A-deficient mice. J. Neurosci. 23, 3953-3959.
42. Schmitt, W. B., Arianpour, R., Deacon, R. M., Seeburg, P. H., Sprengel, R., Rawlins, J. N., and Bannerman, D. M. (2004a). The role of hippocampal glutamate receptor-A-dependent synaptic plasticity in conditional learning: the importance of spatiotemporal discontiguity. J. Neurosci. 24, 7277-7282.
43. Schmitt, W. B., Deacon, R. M., Reisel, D., Sprengel, R., Seeburg, P. H., Rawlins, J. N., and Bannerman, D. M. (2004b). Spatial reference memory in GluR-A-deficient mice using a novel hippocampal-dependent paddling pool escape task. Hippocampus 14, 216-223.
44. Schmitt, W. B., Sprengel, R., Mack, V., Draft, R. W., Seeburg, P. H., Deacon, R. M., Rawlins, J. N., and Bannerman, D. M. (2005). Restoration of spatial working memory by genetic rescue of GluR-A-deficient mice. Nat. Neurosci. 8, 270-272.
45. Shi, S., Hayashi, Y., Esteban, J. A., and Malinow, R. (2001). Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105, 331-343.
46. Sprengel, R. (2006). Role of AMPA receptors in synaptic plasticity. Cell Tissue Res. 326, 447-455.
47. Stephens, D. N., and Mead, A. N. (2003). What role do GluR1 subunits play in drug abuse? Trends Neurosci. 26, 181-182; Author reply 182-183.
48. Wanisch, K., Tang, J., Mederer, A., and Wotjak, C. T. (2005). Trace fear conditioning depends on NMDA receptor activation and protein synthesis within the dorsal hippocampus of mice. Behav. Brain Res. 157, 63-69.
49. Weidholz, L. M., Owen, A. M., Horton, R. E., Feyder, M., Karlsson, R. M., Hefner, K., Sprengel, R., Ceikel, T., Daws, L. C., and Holmes, A. (2007). Mice lacking the AMPA GluR1 receptor exhibit striatal hyperdopaminergia and 'schizophrenia-related' behaviors. Mol. Psychiatry DOI:10.1038/sj.mp.4002056.
50. Yeh, S. H., Mao, S. C., Lin, H. C., and Gean, P. W. (2006). Synaptic expression of glutamate receptor after encoding of fear memory in the rat amygdala. Mol. Pharmacol. 69, 299-308.
51. Zamanillo, D., Sprengel, R., Hvalby, O., Jensen, V., Burnashev, N., Rozov, A., Kaiser, K. M., Koster, H. J., Borchardt, T., Worley, P., Lubke, J., Frotscher, M., Kelly, P. H., Sommer, B., Andersen, P., Seeburg, P. H., and Sakmann, B. (1999). Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 284, 1805-1811.