Hippocampal CA3 NMDA receptors are crucial for adaptive timing of trace eyeblink conditioned response

Journal of Neuroscience

Volumn 26, Issue 5, 2006, Pages 1562-1570

  Kishimoto, Yasushi ^a,b,c   Nakazawa, Kazu ^c,d   Tonegawa, Susumu ^d   Kirino, Yutaka ^b   Kano, Masanobu ^a,e  

^a KANAZAWA UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^e OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Area CA3; Eyeblink conditioning; Hippocampus; Mouse; NMDA receptor; Nonspatial associative memory

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN SUBUNIT;

ANIMAL EXPERIMENT; ARTICLE; AUDITORY STIMULATION; BRAIN REGION; CONDITIONING; CONTROLLED STUDY; EYELID REFLEX; FOLLOW UP; HIPPOCAMPUS; KNOCKOUT MOUSE; MALE; MEMORY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; TIME; WILD TYPE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BLINKING; CONDITIONING, EYELID; ELECTROMYOGRAPHY; EXTINCTION, PSYCHOLOGICAL; HIPPOCAMPUS; KINETICS; MICE; MICE, KNOCKOUT; PYRAMIDAL CELLS; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 32544452992     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4142-05.2006     Document Type: Article

References (48)

1. Abbott LF, Blum KI (1996) Functional significance of long-term potentiation for sequence learning and prediction. Cereb Cortex 6:406-416.
2. August DA, Levy WB (1999) Temporal sequence compression by an integrate-and-fire model of hippocampal area CA3. J Comput Neurosci 6:71-90.
3. Bao S, Chen L, Qiao X, Knusel B, Thompson RF (1998) Impaired eye-blink conditioning in waggler, a mutant mouse with cerebellar BDNF deficiency. Learn Mem 5:355-364.
4. Chan KH, Morell JR, Jarrard LE, Davidson TL (2001) Reconsideration of the role of the hippocampus in learned inhibition. Behav Brain Res 119:111-130.
5. Cho YH, Friedman E, Silva AJ (1999) Ibotanate lesions of the hippocampus impair spatial learning but not contextual fear conditioning in mice. Behav Brain Res 98:77-87.
6. Clark RE, Squire LR (1998) Classical conditioning and brain systems: the role of awareness. Science 280:77-81.
7. Douglas RJ (1967) The hippocampus and behavior. Psychol Bull 67:416-422.
8. Gerlai R (1998) Contextual learning and cue association in fear conditioning in mice: a strain comparison and a lesion study. Behav Brain Res 95:191-203.
9. Gormezano I, Prokasy WF, Thompson RF (1987) Classical conditioning, Ed 3. Boca Raton, FL: CRC.
10. Hasselmo ME, McClelland JL (1999) Neural models of memory. Curr Opin Neurobiol 9:184-188.
11. Hasselmo ME, Schnell E, Barkai E (1995) Dynamics of learning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3. J Neurosci 15:5249-5262.
12. Hasselmo ME, Bodelon C, Wyble BP (2002) A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput 14:793-817.
13. Izquierdo I, Medina JH, Vianna MRM, Izquierdo LA, Barros DM (1999) Separate mechanism for short- and long-term memory. Behav Brain Res 103:1-11.
14. James GO, Hardiman MJ, Yeo CH (1987) Hippocampal lesions and trace conditioning in the rabbit. Behav Brain Res 23:109-116.
15. Jensen O, Lisman JE (1996) Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. Learn Mem 3:279-287.
16. Kadotani H, Hirano T, Masugi M, Nakamura K, Nakao K, Katsuki M, Nakanishi S (1996) Motor discoordination results from combined gene disruption of the NMDA receptor NR2A and NR2C subunits, but not from single disruption of the NR2A or NR2C subunit. J Neurosci 16:7859-7867.
17. Kesner RP, Gilbert PE, Wallenstein GV (2000) Testing neural network models of memory with behavioral experiments. Curr Opin Neurobiol 10:260-265.
18. Kim JJ, Clark RE, Thompson RF (1995) Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. Behav Neurosci 109:195-203.
19. Kimble DP (1968) Hippocampus and internal inhibition. Psychol Bull 70:285-295.
20. Kishimoto Y, Kawahara S, Mori H, Mishina M, Kirino Y (2001) Long-trace interval eyeblink conditioning is impaired in mutant mice lacking the NMDA receptor subunit ε1. Eur J Neurosci 13:1221-1227.
21. Kishimoto Y, Fujimichi R, Araishi K, Kawahara S, Kano M, Aiba A, Kirino Y (2002) mGluR1 in cerebellar Purkinje cells is required for normal association of temporally contiguous stimuli in classical conditioning. Eur J Neurosci 16:2416-2424.
22. Levy WB (1996) A sequence predicting CA3 is a flexible associate that learns and uses context to solve hippocampus-like tasks. Hippocampus 6:579-590.
23. Levy WB, Steward O (1983) Temporal contiguity requirements for long-term associative potentiation/depression in the hippocampus. Neuroscience 8:791-797.
24. Lisman JE (1999) Relating hippocampal circuitry to function: recall of memory sequences by reciprocal dentate-CA3 interactions. Neuron 22:2333-2342.
25. Marr D (1971) Simple memory: a theory for archicortex. Philos Trans R Soc Lond B Biol Sci 262:23-81.
26. McEchron MD, Disterhoft JF (1999) Hippocampal encoding of non-spatial trace conditioning. Hippocampus 9:385-396.
27. McGlinchey-Berroth R, Carrillo MC, Gabrieli JD, Brawn CM, Disterhoft JF (1997) Impaired trace eye-blink conditioning in bilateral, medial-temporal lobe amnesia. Behav Neurosci 111:873-882.
28. Morris RG, McNaughton BL (1987) Hippocampal synaptic enhancement and information-storage within a distributed memory system. Trends Neurosci 10:408-415.
29. Moyer JRJ, Deyo RA, Disterhoft JF (1990) Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behav Neurosci 104:243-252.
30. Myers KM, Davis M (2002) Behavioral and neural analysis of extinction. Neuron 36:567-584.
31. Nakazawa K, Quirk MC, Chitwood RA, Watanabe M, Yeckel MF, Sun LD, Kato A, Carr CA, Johnston DJ, Wilson MA, Tonegawa S (2002) Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 297:211-218.
32. Nakazawa K, Sun LD, Quirk MC, Rondi-Reig L, Wilson MA, Tonegawa S (2003) Hippocampal CA3 NMDA receptors are crucial for memory acquisition of one-time experience. Neuron 38:305-315.
33. Nakazawa K, McHugh TJ, Wilson MA, Tonegawa S (2004) NMDA receptors, place cells and hippocampal spatial memory. Nat Rev Neurosci 5:361-372.
34. Niki H (1966) Response preservation following hippocampal ablation in the rat. Jpn Psychol Res 8:1-9.
35. Pavlov IP (1927) Conditioned reflexes. London: Oxford UP.
36. Port RL, Romano AG, Steinmetz JE, Mikhail AA, Patterson MM (1986) Retention and acquisition of classical trace conditioned responses by rabbits with hippocampal lesions. Behav Neurosci 100:745-752.
37. Rodriguez P, Levy WB (2001) A model of hippocampal activity in trace conditioning: where' s the trace? Behav Neurosci 115:1224 -1238.
38. Sakamoto T, Takatsuki K, Kawahara S, Kirino Y, Niki H, Mishina M (2005) Role of hippocampal NMDA receptors in trace eyeblink conditioning. Brain Res 1039:130-136.
39. Solomon PR, Vander Schaaf EV, Thompson RF, Weisz DJ (1986) Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behav Neurosci 100:729-744.
40. Szapiro G, Vianna MR, McGaugh JL, Medina JH, Izquierdo I (2003) The role of NMDA glutamate receptors, PKA, MAPK, and CaMKII in the hippocampus in extinction of conditioned fear. Hippocampus 13:53-58.
41. Takatsuki K, Kawahara S, Takehara K, Kishimoto Y, Kirino Y (2001) Effects of the noncompetitive NMDA receptor antagonist MK-801 on classical eyeblink conditioning in mice. Neuropharmacology 41:618-628.
42. Thompson LT, Disterhoft JF (1997) N-methyl-D-aspartate receptors in associate eyeblink conditioning: both MK-801 and phencyclidine produce task- and dose-dependent impairments. J Pharmacol Exp Ther 281:928-940.
43. Thompson RF, Kim JJ (1996) Memory systems in the brain and localization of a memory. Proc Natl Acad Sci USA 93:13438-13444.
44. Thompson RF, Bao S, Chen L, Cipriano BD, Grethe JS, Kim JJ, Thompson JK, Tracy JA, Weninger MS, Krupa DJ (1997) Associative learning. San Diego: Academic.
45. Tseng W, Guan R, Disterhoft JF, Weiss C (2004) Trace eyeblink conditioning is hippocampally dependent in mice. Hippocampus 14:58-65.
46. Wallenstein GV, Eichenbaum H, Hasseimo ME (1998) The hippocampus as an associator of discontiguous events. Trends Neurosci 21:317-323.
47. Weiss C, Bouwmeester H, Power JM, Disterhoft JF (1999) Hippocampal lesions prevent trace eyeblink conditioning in the freely moving rat. Behav Brain Res 99:123-132.
48. Yeo C, Hesslow G (1998) Cerebellum and conditioned reflexes. Trends Cogn Sci 2:322-330.