Circuit mechanisms of GluA1-dependent spatial working memory

Hippocampus

Volumn 23, Issue 12, 2013, Pages 1359-1366

  Freudenberg, Florian ^a,b,d   Marx, Verena ^a,b   Seeburg, Peter H ^b   Sprengel, Rolf ^b   Celikel, Tansu ^a,c  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

^c RADBOUD UNIVERSITY   (Netherlands)

^d UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

AMPA; Gene targeting; GluA1; Neural circuits; Spatial working memory

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMINO ACID; AMPA RECEPTOR; GLUA1 PROTEIN; GLUTAMIC ACID; LEUCINE; UNCLASSIFIED DRUG;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; CONTROLLED STUDY; FEMALE; FOREBRAIN; HIPPOCAMPUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPATIAL MEMORY; SPATIAL WORKING MEMORY; WORKING MEMORY;

AMPA; GENE TARGETING; GLUA1; NEURAL CIRCUITS; SPATIAL WORKING MEMORY;

ANIMALS; CONDITIONING, CLASSICAL; FEAR; FEMALE; HIPPOCAMPUS; MALE; MAZE LEARNING; MEMORY, SHORT-TERM; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE NET; PHOSPHOPYRUVATE HYDRATASE; PROSENCEPHALON; RECEPTORS, AMPA; SPACE PERCEPTION; STEREOTAXIC TECHNIQUES;

EID: 84888135991     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22184     Document Type: Article

References (54)

1. Allen CB, Celikel T, Feldman DE. 2003. Long-term depression induced by sensory deprivation during cortical map plasticity in vivo. Nature Neurosci 6:291-299.
2. Anagnostaras SG, Gale GD, Fanselow MS. 2001. Hippocampus and contextual fear conditioning: Recent controversies and advances. Hippocampus 11:8-17.
3. Bannerman DM, Deacon RMJ, Brady S, Bruce A, Sprengel R, Seeburg PH, Rawlins JNP. 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.
4. Bannerman DM, Deacon RMJ, Offen S, Friswell J, Grubb M, Rawlins JNP. 2002. Double dissociation of function within the hippocampus: Spatial memory and hyponeophagia. Behav Neurosci 116:884-901.
5. Bannerman DM, Niewoehner B, Lyon L, Romberg C, Schmitt WB, Taylor A, Sanderson DJ, Cottam J, Sprengel R, Seeburg PH, Kohr G, Rawlins JNP. 2008. NMDA Receptor subunit NR2A is required for rapidly acquired spatial working memory but not incremental spatial reference memory. J Neurosci 28:3623-3630.
6. Bannerman DM, Yee BK, Good MA, Heupel MJ, Iversen SD, Rawlins JN. 1999. Double dissociation of function within the hippocampus: A comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions. Behav Neurosci 113:1170-1188.
7. Bannerman DM, Yee BK, Lemaire M, Wilbrecht L, Jarrard L, Iversen SD, Rawlins JN, Good MA. 2001. The role of the entorhinal cortex in two forms of spatial learning and memory. Exp Brain Res 141:281-303.
8. Cai C, Coleman SK, Niemi K, Keinänen K. 2002. Selective binding of synapse-associated protein 97 to GluR-A alpha-amino-5-hydroxy-3-methyl-4-isoxazole propionate receptor subunit is determined by a novel sequence motif. J Biol Chem 277:31484-31490.
9. Celikel T, Marx V, Freudenberg F, Zivkovic A, Resnik E, Hasan MT, Licznerski P, Osten P, Rozov A, Seeburg PH, Schwarz MK. 2007. Select overexpression of homer1a in dorsal hippocampus impairs spatial working memory. Frontiers Neurosci 1:97-110.
10. Celikel T, Sakmann B. 2007. Sensory integration across space and in time for decision making in the somatosensory system of rodents. Proc Natl Acad Sci USA 104:1395-1400.
11. Celikel T, Szostak VA, Feldman DE. 2004. Modulation of spike timing by sensory deprivation during induction of cortical map plasticity. Nat Neurosci 7:534-541.
12. Clem RL, Barth A. 2006. Pathway-specific trafficking of native AMPARs by in vivo experience. Neuron 49:663-670.
13. Clem RL, Celikel T, Barth AL. 2008. Ongoing in vivo experience triggers synaptic metaplasticity in the neocortex. Science 319:101-104.
14. Constantinidis C, Wang X-J. 2004. A neural circuit basis for spatial working memory. Neuroscientist 10:553-565.
15. Corsini NS, Sancho-Martinez I, Laudenklos S, Glagow D, Kumar S, Letellier E, Koch P, Teodorczyk M, Kleber S, Klussmann S, Wiestler B, Brüstle O, Mueller W, Gieffers C, Hill O, Thiemann M, Seedorf M, Gretz N, Sprengel R, Celikel T, Martin-Villalba A. 2009. The death receptor CD95 activates adult neural stem cells for working memory formation and brain repair. Cell Stem Cell 5:178-190.
16. Deacon RMJ, Rawlins JNP. 2006. T-maze alternation in the rodent. Nat Protocols 1:7-12.
17. Von Engelhardt J, Doganci B, Jensen V, Hvalby Ø, Göngrich C, Taylor A, Barkus C, Sanderson DJ, Rawlins JNP, Seeburg PH, Bannerman DM, Monyer H. 2008. Contribution of hippocampal and extra-hippocampal NR2B-containing NMDA receptors to performance on spatial learning tasks. Neuron 60:846-860.
18. Feyder M, Wiedholz L, Sprengel R, Holmes A. 2007. Impaired associative fear learning in mice with complete loss or haploinsufficiency of AMPA GluR1 receptors. Frontiers Behav Neurosci 1:1-5.
19. Freudenberg F, Marx V, Mack V, Layer LE, Klugmann M, Seeburg PH, Sprengel R, Celikel T. 2013. GluA1 and its PDZ-interaction: A role in experience-dependent behavioral plasticity in the forced swim test. Neurobiol Dis 52:160-167.
20. Freund T, Buszáki G. 1996. Interneurons of the hippocampus. Hippocampus 470:347-470.
21. Fuchs EC, Zivkovic AR, Cunningham MO, Middleton S, Lebeau FEN, Bannerman DM, Rozov A, Whittington MA, Traub RD, Rawlins JNP, Monyer H. 2007. Recruitment of parvalbumin-positive interneurons determines hippocampal function and associated behavior. Neuron 53:591-604.
22. Good M, Honey RC. 1997. Dissociable effects of selective lesions to hippocampal subsystems on exploratory behavior, contextual learning, and spatial learning. Behav Neurosci 111:487-493.
23. Van Haaren F, de Bruin J, Heinsbroek R, van de Poll N. 1985. Delayed spatial response alternation: effects of delay-interval duration and lesions of the medial prefrontal cortex on response accuracy of male and female Wistar rats. Behav Brain 18:41-49.
24. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R. 2000. Driving AMPA receptors into synapses by LTP and CaMKII: Requirement for GluR1 and PDZ domain interaction. Science 287:2262-2267.
25. Hock BJ, Bunsey MD. 1998. Differential effects of dorsal and ventral hippocampal lesions. J Neurosci 18:7027-7032.
26. Humeau Y, Reisel D, Johnson AW, Borchardt T, Jensen V, Gebhardt C, Bosch V, Gass P, Bannerman DM, Good MA, Hvalby Ø, Sprengel R, Lüthi A. 2007. A pathway-specific function for different AMPA receptor subunits in amygdala long-term potentiation and fear conditioning. J Neurosci 27:10947-10956.
27. Jensen V, Kaiser KMM, Borchardt T, Adelmann G, Rozov A, Burnashev N, Brix C, Frotscher M, Andersen P, Hvalby Ø, Sakmann B, Seeburg PH, Sprengel R. 2003. A juvenile form of postsynaptic hippocampal long-term potentiation in mice deficient for the AMPA receptor subunit GluR-A. J Physiol 553:843-856.
28. Kesner RP, Bolland BL, Dakis M. 1993. Memory for spatial locations, motor responses, and objects: Triple dissociation among the hippocampus, caudate nucleus, and extrastriate visual cortex. Exp Brain Res 462-470.
29. Kessels HW, Malinow R. 2009. Synaptic AMPA receptor plasticity and behavior. Neuron 61:340-350.
30. Kjelstrup KG, Tuvnes FA, Steffenach H-A, Murison R, Moser EI, Moser M-B. 2002. Reduced fear expression after lesions of the ventral hippocampus. Proc Natl Acad Sci USA 99:10825-10830.
31. Kullmann D. 2011. Interneuron networks in the hippocampus. Current Opin Neurobiol 21:709-716.
32. Lee I, Kesner RP. 2003. Time-dependent relationship between the dorsal hippocampus and the prefrontal cortex in spatial memory. J Neurosci 23:1517-1523.
33. Leonard AS, Davare MA, Horne M, Garner CC, Hell JW. 1998. SAP97 is associated with the α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor GluR1 subunit. J Biol Chem 273:19518-19524.
34. 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.
35. Mack V, Burnashev N, Kaiser KM, Rozov A, Jensen V, Hvalby O, Seeburg PH, Sakmann B, Sprengel R. 2001. Conditional restoration of hippocampal synaptic potentiation in Glur-A-deficient mice. Science 292:2501-2504.
36. Mogensen J, Hjortkjaer J, Ibervang KL, Stedal K, Malá H. 2007. Prefrontal cortex and hippocampus in posttraumatic functional recovery: Spatial delayed alternation by rats subjected to transection of the fimbria-fornix and/or ablation of the prefrontal cortex. Brain Res Bull 73:86-95.
37. Ramirez JJ, Stein DG. 1984. Sparing and recovery of spatial alternation performance after entorhinal cortex lesions in rats. Behav Brain Res 13:53-61.
38. Reisel D, Bannerman DM, Schmitt WB, Deacon RMJ, Flint J, Borchardt T, Seeburg PH, Rawlins JNP. 2002. Spatial memory dissociations in mice lacking GluR1. Nat Neurosci 5:868-873.
39. Richmond MA, Yee BK, Pouzet B, Veenman L, Rawlins JN, Feldon J, Bannerman DM. 1999. Dissociating context and space within the hippocampus: Effects of complete, dorsal, and ventral excitotoxic hippocampal lesions on conditioned freezing and spatial learning. Behav Neurosci 113:1189-1203.
40. Rogers SW, Hughes TE, Hollmann M, Gasic GP, Deneris ES, Heinemann S. 1991. The characterization and localization of the glutamate receptor subunit GluRl in the rat brain. J Neurosci 11:2713-2724.
41. Sanderson DJ, Good MA, Seeburg PH, Sprengel R, Rawlins JNP, Bannerman DM. 2008. The role of the GluR-A (GluR1) AMPA receptor subunit in learning and memory. In: Sossin W, Lacaille J-C, Castellucci V, Belleville S, editors. Progress in Brain Research, Vol. 169. Elsevier. pp 159-178.
42. Sans N, Racca C, Petralia RS, Wang Y-X, McCallum J, Wenthold RJ. 2001. Synapse-associated protein 97 selectively associates with a subset of AMPA receptors early in their biosynthetic pathway. J Neurosci 21:7506-7516.
43. Schmitt WB, Sprengel R, Mack V, Draft RW, Seeburg PH, Deacon RMJ, Rawlins JNP, Bannerman DM. 2005. Restoration of spatial working memory by genetic rescue of GluR-A-deficient mice. Nat Neurosci 8:270-272.
44. Schwabe K, Enkel T, Klein S, Schütte M, Koch M. 2004. Effects of neonatal lesions of the medial prefrontal cortex on adult rat behaviour. Behav Brain Res 153:21-34.
45. Seib DRM, Corsini NS, Ellwanger K, Plaas C, Mateos A, Pitzer C, Niehrs C, Celikel T, Martin-Villalba A. 2013. Loss of dickkopf-1 restores neurogenesis in old age and counteracts cognitive decline. Cell Stem Cell 12:204-214.
46. Shaw C, Aggleton JP. 1993. The effects of fornix and medial prefrontal lesions on delayed non-matching-to-sample by rats. Behav Brain Res 54:91-102.
47. Shi S, Hayashi Y, Esteban JA, Malinow R. 2001. Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105:331-343.
48. Shimshek D, Kim J, Hübner M, Spergel DJ, Buchholz F, Casanova E, Stewart AF, Seeburg PH, Sprengel R. 2002. Codon-improved Cre recombinase (iCre) expression in the mouse. Genesis 32:19-26.
49. Shimshek DR, Jensen V, Celikel T, Geng Y, Schupp B, Bus T, Mack V, Marx V, Hvalby Ø, Seeburg PH, Sprengel R. 2006. Forebrain-specific glutamate receptor B deletion impairs spatial memory but not hippocampal field long-term potentiation. J Neurosci 26:8428-8440.
50. Songyang Z, Fanning A, Fu C, Xu J, Marfatia S, Chishti A, Crompton A, Chan A, Anderson J, Cantley L. 1997. Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science 275:73-77.
51. Voigts J, Sakmann B, Celikel T. 2008. Unsupervised whisker tracking in unrestrained behaving animals. J Neurophysiol 100:504-515.
52. Wiedholz LM, Owens WA, Horton RE, Feyder M, Karlsson R-M, Hefner K, Sprengel R, Celikel T, Daws LC, Holmes A. 2008. Mice lacking the AMPA GluR1 receptor exhibit striatal hyperdopaminergia and "schizophrenia-related" behaviors. Mol Psychiatry 13:631-640.
53. Zamanillo D, Sprengel R, Hvalby O, Jensen V, Burnashev N, Rozov A, Kaiser KM, Köster HJ, Borchardt T, Worley P, Lübke J, Frotscher M, Kelly PH, Sommer B, Andersen P, Seeburg PH, Sakmann B. 1999. Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 284:1805-1811.
54. Zimmer HD. 2008. Visual and spatial working memory: from boxes to networks. Neurosci Biobehav Rev 32:1373-1395.