Differential effects of ibotenic acid lesions of the hippocampus and blockade of N-methyl-D-aspartate receptor-dependent long-term potentiation on contextual processing in rats

Behavioral Neuroscience

Volumn 111, Issue 6, 1997, Pages 1171-1183

  Good, Mark ^a,b   Bannerman, David ^a,c  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

IBOTENIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; VALERIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; APPETITE; ARTICLE; CONDITIONING; CONTROLLED STUDY; DRUG EFFECT; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIPPOCAMPUS; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; RAT; RECEPTOR BLOCKING; STIMULUS RESPONSE; SYNAPTIC TRANSMISSION; TASK PERFORMANCE;

2-AMINO-5-PHOSPHONOVALERATE; ANIMALS; APPETITIVE BEHAVIOR; CONDITIONING (PSYCHOLOGY); CUES; DISCRIMINATION LEARNING; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; IBOTENIC ACID; INFUSION PUMPS, IMPLANTABLE; LONG-TERM POTENTIATION; MALE; MEMORY; RATS; RATS, INBRED STRAINS; RECEPTORS, N-METHYL-D-ASPARTATE; STEREOTAXIC TECHNIQUES;

EID: 0031463865     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/0735-7044.111.6.1171     Document Type: Article

References (64)

1. Abeliovich, A., Chen, C., Goda, Y., Paylor, R., McKee, A., Shuster, L., Wehner, J., Stevens, C. F., & Tonegawa, S. (1993). PKC-γ mutant mice exhibit mild deficits in spatial and contextual learning. Cell, 75, 1263-1271.
2. Bannerman, D. M., Good, M. A., Butcher, S. P., Ramsey, M., & Morris, R. G. M. (1995a). Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature, 378, 182-186.
3. Bannerman, D. M., Good, M. A., Butcher, S. P., Ramsey, M., & Morris, R. G. M. (1995b). NMDA receptors, long-tenu potentiation and spatial learning. Brain Research Association Abstracts, 12, 107.
4. Bliss, T. V. P., & Collingridge, G. L. (1993). A synaptic model of memory: Long-term potentiation in the hippocampus. Nature, 361, 31-39.
5. Bliss, T. V. P., & Lømo, T. (1973). Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetised rabbit following stimulation of the perforant path. Journal of Physiology, 232, 331-356.
6. Bonardi, C., Honey, R. C, & Hall, G. (1990). Context specificity of conditioning in flavour-aversion learning: Extinction and blocking tests. Animal Learning & Behavior, 18, 229-237.
7. Bourtchuladze, R., Frenguelli, B., Blendy, J., Cioffi, D., Schutz, G., & Silva, A. J. (1994). Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell, 79, 59-68.
8. Bouton, M. E. (1993). Context, time, and memory retrieval in the interference paradigms of Pavlovian learning. Psychological Bulletin, 114, 80-99.
9. Bouton, M. E., & Bolles, R. C. (1985). Contexts, event memories, and extinction. In P. D. Balsam & A. Tomie (Eds.), Context and learning (pp. 133-166). Hillsdale, NJ: Erlbaum.
10. Bouton, M. E., & Peck, C. A. (1989). Contexts effects on conditioning, extinction and reinstatement in an appetitive conditioning preparation. Animal Learning & Behavior, 17, 188-198.
11. Bouton, M. E., & Swartzentruber, D. (1986). Analysis of the associative and occasion-setting properties of contexts participating in a Pavlovian discrimination. Journal of Experimental Psychology: Animal Behavior Processes, 12, 333-350.
12. Butcher, S. P., & Hamberger, A. (1987). In vivo studies on the extracellular, and veratrine-releasable. pools of endogenous amino acids in the rat striatum: Effects of corticostriatal deafferentation and kainic acid lesion. Journal of Neurochemistry, 48, 713-721.
13. Butcher, S. P., Hamberger, A., & Morris, R. G. M. (1991). Intracerebral distribution of D,L-2-amino-phosphonopentanoic acid (AP5) and the dissociation of different types of learning. Experimental Brain Research, 83, 521-526.
14. Cahill, L., & McGaugh, J. L. (1990). Amygdaloid complex lesions differentially affect retention of tasks using appetitive and aversive reinforcement. Behavioral Neuroscience, 104, 532-543.
15. Cahusac, P. M. B., Evans, R. H., Hill, R. G., Rodriguez, R. E., & Smith, D. A. S. (1984). The behavioural effect of an N-methyl-Daspartate antagonist following application to the lumbar spinal cord of conscious rats. Neuropharmacology, 23, 719-724.
16. Cain, D. P., Saucier, D., Hall, J., Hargreaves, E. L., & Boon, F. (1996). Detailed behavioral analysis of watermaze acquisition under APV or CNQX: Contribution of sensorimotor disturbances to drug-induced acquisition deficits. Behavioral Neuroscience, 110, 86-102.
17. Channell, S., & Hall, G. (1983). Contextual effects in latent inhibition with an appetitive conditioning procedure. Animal Learning & Behavior, 11, 67-74.
18. Collingridge, G. L., Kehl, S. J., & McLennan, H. (1983). Excitatory synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. Journal of Physiology, 334, 33-46.
19. Davis, S., Butcher, S. P., & Morris, R. G. M. (1992). The NMDA receptor antagonist D-2-amino-5-phosphonopentanoate (D-AP5) impairs spatial learning and LTP in vivo at intracerebral concentrations comparable to those that block LTP in vitro. Journal of Neuroscience, 12, 21-34.
20. Deisseroth, K., Bito, H., & Tsien, R. W. (1996). Signalling from synapse to nucleus: Post synaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron, 16, 89-101.
21. Deutsch, J. A. (1994). Spatial learning in mutant mice. Science, 262, 760-761.
22. Fanselow, M. S., Kim, J. J., Yipp, J., & DC Oca, B. (1994). Differential effects of the N-methyl-D-aspartate antagonist D,L-2amino-5-phosphonovalerate on acquisition of fear of auditory and contextual cues. Behavioral Neuroscience, 108, 235-240.
23. Gerlai, R. (1996). Gene-targeting studies of mammalian behavior: Is it the mutation or the background genotype? Trends in Neurosciences, 19, 177-181.
24. Grant, S. G. N., O'Dell, T. J., Karl, K. A., Stein, P. L., Soriano, P., & Kandel, E. R. (1992). Tyrosine kinases and long-term potentiation: Impaired spatial learning in Fyn mutant mice. Science, 258, 1903-1910.
25. Hall, G., & Honey, R. C. (1989). Contextual effects in conditioning, latent inhibition, and habituation: Associative and retrieval functions of contextual cues. Journal of Experimental Psychology: Animal Behavior Processes, 15, 232-241.
26. Hall, G., & Honey, R. C. (1990). Context-specific conditioning in a conditioned-emotional-response procedure. Journal of Experimental Psychology: Animal Behavior Processes, 16, 271-278.
27. Hall, G., & Pearce, J. M. (1979). Latent inhibition of a CS during CS-UCS pairings. Journal of Experimental Psychology: Animal Behavior Processes, 5, 31-42.
28. Hebb, D. O. (1949). The organization of behavior: A neuropsychological theory. New York: Wiley.
29. Hirsh, R. (1974). The hippocampus and contextual retrieval of information from memory: A theory. Physiological Psychology, 8, 175-182.
30. Honey, R. C., & Good, M. (1993). Selective hippocampal lesions abolish the contextual specificity of latent inhibition and conditioning. Behavioral Neuroscience, 107, 23-33.
31. Honey, R. C., Willis, A., & Hall, G. (1990). Context specificity in pigeon autoshaping. Learning and Motivation, 21, 125-136.
32. Jarrard, L. E. (1989). On the use of ibotenic acid to lesion selectively different components of the hippocampal formation. Journal of Neuroscience Methods, 29, 251-259.
33. Keith, J. R., & Rudy, J. W. (1990). Why NMDA receptor-dependent long-term potentiation may not be a mechanism of learning and memory: Reappraisal of the NMDA-receptor blockade strategy. Psychobiology, 18, 251-259.
34. Kim, J. J., DeCola, J. P., Landeira-Fernandez, J., & Fanselow, M. S. (1991). N-methyl-D-aspartate antagonist AP5 blocks acquisition but not expression of fear conditioning. Behavioral Neuroscience, 107, 1093-1098.
35. Kim, J. J., & Fanselow, M. S. (1992). Modality specific retrograde amnesia of fear following hippocampal lesions. Science, 256, 675-677.
36. Lindroth, P., & Mopper, K. (1979). High performance liquid Chromatographic determination of subpicomole amounts of amino acids by precolumn fluorescence derivitization with ω-phthaldialdehyde. Analytical Chemistry, 51, 1667-1674.
37. Medin, D. L., (1976). Animal models and memory models. In D. L. Medin, W. A. Roberts. & R. T. Davis (Eds.), Processes of animal memory (pp. 113-134). Hillsdale, NJ: Erlbaum.
38. Morris, R. G. M. (1989). Synaptic plasticity and learning: Selective impairment of learning in rats and blockade of long-term potentiation in vivo by the N-methyl-D aspartate receptor antagonist AP5. Journal of Neuroscience, 9, 3040-3057.
39. Morris, R. G. M., Andersen, E., Lynch, G., & Baudry, M. (1986). Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature, 319, 774-776.
40. Morris, R. G. M., & Davis, M (1994). The role of NMDA receptors in learning and memory. In G. L. Collingridge & J. C. Watkins (Eds.), The NMDA receptor (2nd ed., pp. 340-375). Oxford, England: Oxford University Press.
41. Morris, R. G. M., Davis, S., & Butcher, S. P. (1990). Hippocampal synaptic plasticity and NMDA receptors: A role in information storage? Philosophical Transactions of The Royal Society of London (Section B), 329, 187-204.
42. Morris, R. G. M., Garrud, P., Rawlins, J. N. P., & O'Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature, 297, 681-683.
43. Morris, R. G. M., Hagan, J. J., & Rawlins, J. N. P. (1986). Allocentric spatial learning by hippocampectomised rats: A further test of the spatial-mapping and working-memory theories of hippocampal function. Quarterly Journal of Experimental Psychology, 38B, 365-395.
44. Morris, R. G. M., Halliwell, R. F., & Bowery, N. (1989). Synaptic plasticity and learning: II. Do different kinds of plasticity underlie different kinds of learning? Neuropsychologia, 27, 41-59.
45. Morris, R. G. M., & Kennedy, M. B. (1992) The Pierian spring. Current Biology, 2, 511-514.
46. Morris, R. G. M., Schenk, F., Tweedie, F., & Jarrard, L. E. (1990). Ibotenate lesions of hippocampus and/or subiculum: Dissociating components of allocentric spatial learning. European Journal of Neuroscience, 2, 1016-1028.
47. O'Keefe, J., & Nadel, L. (1978). The hippocampus as a cognitive map. Oxford. England: Oxford University Press.
48. Olton, D. S., Becker, J. T. & Handelman, G. E. (1979). Hippocampus, space and memory. Behavioral and Brain Sciences, 2, 315-365.
49. Paxinos, G., & Watson, C. (1986). The rat brain in stereotaxic coordinates. San Diego, CA: Academic Press.
50. Phillips, R. G., & LeDoux, J. E. (1992). Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behavioral Neuroscience, 106, 274-285.
51. Phillips, R. G.. & LeDoux, J. F. (1994). Lesions of the dorsal hippocampal formation interfere with background but not foreground contextual fear conditioning. Learning and Memory, 1, 34-44.
52. Sakimura, K., Kutsuwada, T, Ito, I., Manabe, T., Takayama, C., Kushiya, E., Yagi, T., Aizawa, S., Inouc, Y., Sugiyama, H., & Mishina, M. (1995). Reduced hippocampal LTP and spatial learning in mice lacking NMDA receptor el subunit. Nature, 373, 151-155.
53. Saucier, D., & Cain, D. P. (1995). Spatial learning without NMDA receptor-dependent long-term potentiation. Nature, 378, 186-189.
54. Saucier, D., Hargreaves, E. L., Boon, F., Vanderwolf, C. H., & Cain, D. P. (1996). Detailed behavioral analysis of watermaze acquisition under systemic NMDA or muscarinic antagonism: Nonspatial pretraining eliminates spatial learning deficits. Behavioral Neuroscience, 110, 103-116.
55. Silva, A. J., Paylor, R., Wehner, J. M., & Tonegawa, S. (1992). Impaired spatial learning in a calcium-calmodulin kinase II mutant mice. Science, 257, 206-211.
56. Silva, A. J., Stevens, C. F., Tonegawa, S., & Wang, Y. (1992). Deficient long-term potentiation in a-calcium-calmodulin kinase II mutant mice. Science, 257, 201-206.
57. Shapiro, M. L., & Caramanos, Z. (1990). NMDA antagonist MK-801 impairs acquisition but not performance of spatial working and reference memory. Psychobiology, 18, 231-243.
58. Tonkiss, J., Morris, R. G. M., & Rawlins, J. N. P. (1988). Intraventricular infusion of the NMDA antagonist AP5 impairs performance on a non-spatial operant DRL task in the rat. Experimental Brain Research, 73, 181-188.
59. Tully, T., Preat, T., Boynton, S. C., & Del Vecchio, M. (1994). Genetic dissection of consolidated memory in Drosophila. Cell, 79, 35-47.
60. Wagner, A. R. (1976). Priming in STM: An information processing mechanism for self-generated and retrieval-generated depression in performance. In T. J. Tighe & R. N. Leaton (Eds.), Habituation: Perspectives from child development, animal behavior, and neurophysiology (pp. 95-128). Hillsdale, NJ: Erlbaum.
61. Wagner, A. R. (1978). Expectancies and the priming of STM. In S. H. Hulse, H. Fowler, & W. K. Honig (Eds.), Cognitive aspects of animal behavior (pp. 177-209). Hillsdale, NJ: Erlbaum.
62. Wagner, A. R. (1981). SOP: A model of automatic memory processing in animal behavior. In N. E. Spear & R. R. Miller (Eds.). Information processing in animals: Memory mechanisms (pp. 5-47). Hillsdale, NJ: Erlbaum.
63. Yin, J. C. P., Wallach, J. S., Del Vecchio, M. Wilder, E. L., Zhou. H., Quinn, W. G., & Tully, T. (1994). Induction of a dominantnegative CREB transgene blocks long-term memory in Drosophila. Cell, 79, 49-58.
64. Young, S. L., Bohenek, D. L., & Fanselow, M. S. (1994). NMDA processes mediate anterograde amnesia of contextual fear conditioning induced by hippocampal damage: Immunization against amnesia by context preexposure. Behavioral Neuroscience, 108, 19-29.