N-methyl-D-aspartate receptors in associative eyeblink conditioning: Both MK-801 and phencyclidine produce task-and dose-dependent impairments

Journal of Pharmacology and Experimental Therapeutics

Volumn 281, Issue 2, 1997, Pages 928-940

  Thompson, Lucien T ^a   Disterhoft, John F ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIZOCILPINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PHENCYCLIDINE;

ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; BLINKING; CONDITIONING; DISEASE SEVERITY; DRUG ABUSE; EYELID REFLEX; HIPPOCAMPUS; LEARNING; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; RABBIT; STATISTICAL ANALYSIS; TASK PERFORMANCE;

ANIMALS; CONDITIONING, EYELID; DIZOCILPINE MALEATE; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; PHENCYCLIDINE; RABBITS; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 0030974183     PISSN: 00223565     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (103)

1. ADEY, W. R. AND DUNLOP, L. W.: The action of certain cyclohexamines on hippocampal system during approach performance in the cat. J. Pharmacol. Exp. Ther. 130: 418-426, 1960.
2. AKASE, E., ALKON, D. L. AND DISTERHOFT, J. F.: Hippocampal lesions impair memory of short-delay conditioned eyeblink in rabbits. Behav. Neurosci. 103: 935-943, 1989.
3. AKASE, E., THOMPSON, L. T. AND DISTERHOFT, J. F.: A system for quantitative analysis of associative learning: 2. Real-time software for MS-DOS microcomputers. J. Neurosci. Methods 54: 119-130, 1994.
4. ALLAOUA, H. AND CHICHEPORTICHE, R.: Anaesthetic properties of phencyclidine (PCP) and analogues may be related to their interaction with Na+ channels. Eur. J. Pharmacol. 163: 327-335, 1989.
5. ALLEN, M. R. AND YOUNG, S. J.: Phencyclidine-induced psychosis. Am. J. Psychiat. 135: 1081-1084, 1978.
6. ANDERSEN, P.: Long-term potentiation-Outstanding problems. In The Neural and Molecular Bases of Learning, ed. by J.-P. Changeux and M. Konishi, pp. 239-262, Wiley, New York, 1987.
7. BARNES, C. A.: Involvement of LTP in memory: Are we "searching under the street light"? Neuron 15: 751-754, 1995.
8. BLISS, T. V. P. AND GARDNER-MEDWIN, A. R.: Long-lasting increases of synaptic influence in the unanaesthetized hippocampus. J. Physiol. (Lond.) 216: 32P-33P, 1971.
9. COAN, E. J. AND COLLINGRIDGE, G. L.: Effects of phencyclidine, SKF 10,047 and related psychotomimetic agents on N-methyl-D-aspartate receptor mediated synaptic responses in rat hippocampal slices. Br. J. Pharmacol. 91: 547-556, 1987.
10. COLLINGRIDGE, G. L. AND LESTER, R. A. J.: Excitatory amino acid receptors in the vertebrate central nervous system. Pharmacol. Rev. 41: 143-210, 1989.
11. COLLINGRIDGE, G. L., KEHL, S. J. AND MCLENNAN, H.: Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J. Physiol. (Lond.) 334: 33-46, 1983.
12. CONTRERAS, P. C.: D-serine antagonized phencyclidine and MK-801-induced stereotyped behavior and ataxia. Neuropharmacology 29: 291-293, 1990.
13. DESMOND, N. L., COLBERT, C. M., DE, X. Z. AND LEVY, W. B.: NMDA receptor anatagonists block the induction of long-term depression in the hippocampal dentate gyrus of the anesthetized rat. Brain Res. 552: 93-98, 1991.
14. DINGLEDINE, R., MCBAIN, C. J. AND MCNAMARA, J. O.: Excitatory amino acid receptors in epilepsy. Trends Pharmacol. Sci. 11: 334-338, 1990.
15. DISTERHOFT, J. F. AND BUCHWALD, J. E.: Mapping learning in the brain. In Biology of Reinforcement, ed. by A. Routtenberg, pp. 53-80, Academic Press, New York, 1980.
16. DOMINO, E. F.: Comparison of phencyclidine and related substances with various indole, phenylamine, and other psychotomimetics. Psychopharmacol. Bull. 22: 973-976, 1986.
17. DOMINO, E. F.: Neurobiology of phencyclidine (Sernyl), a drug with an unusual spectrum of pharmacological activity. Int. Rev. Neurobiol. 6: 303-347, 1964.
18. DOUGLAS, R. J.: The hippocampus and behavior. Psychol. Bull. 67: 416-442, 1967.
19. EBERT, B., WONG, E. H. F. AND KROGSGAARD-LARSEN, P.: Identification of a novel NMDA receptor in rat cerebellum. Eur. J. Pharmacol. 208: 49-52, 1991.
20. FAGG, G. E.: Phencyclidine and related drugs bind to the activated N-methyl-D-aspartate receptor-channel complex in the rat brain membranes. Neurosci. Lett. 76: 221-227, 1987.
21. FANSELOW, M. S., KIM, J. J., YIPP, J. AND DE OCA, B.: Differential effects of the N-methyl-D-aspartate antagonist dl-2-amino-5-phosphonovalerate on acquisition of fear of auditory and contextual cues. Behav. Neurosci. 108: 235-240, 1994.
22. FFRENCH-MULLEN, J. M. H. AND ROGAWSKI, M. A.: Interaction of phencyclidine with voltage-dependent potassium channels in cultured rat hippocampal neurons: Comparisons with block of the NMDA receptor-ionophore complex. J. Neurosci. 9: 4051-4061, 1989.
23. FFRENCH-MULLEN, J. M. H. AND ROGAWSKI, M. A.: Phencyclidine block of calcium current in isolated guinea-pig hippocampal neurones. J. Physiol. 456: 85-105, 1992.
24. GORMEZANO, I., PROKASY, W. F. AND THOMPSON, R. F.: Classical Conditioning. Lawrence Erlbaum Assoc., Hillsdale, NJ, 1987.
25. GUNDLACH, A. L., LARGENT, B. L. AND SNYDER, S. H.: Phencyclidine and sigma opiate receptors in brain: Biochemical and autoradiographical differentiation. Eur. J. Pharmacol. 113: 465-466, 1985.
26. HANDELMANN, G. E., CONTRERAS, P. C. AND O'DONOHUE, T. L.: Selective memory impairment by phencyclidine in rats. Eur. J. Pharmacol. 140: 69-73, 1987.
27. HEALE, V. AND HARLEY, C.: MK-801 and AP5 impair acquisition, but not retention, of the Morris milk maze. Pharmacol. Biochem. Behav. 36: 145-149, 1990.
28. HERBERG, L. J. AND ROSE, I. C.: Effects of D-cycloserine and cycloleucine, ligands for the NMDA-associated strychnine-insensitive glycine site, on brain-stimulation reward and spontaneous locomotion. Pharmacol. Biochem. Behav. 36: 735-738, 1990.
29. HIMORI, N., WATANABE, H., AKAIKE, N., KURASAWA, M., ITOH, J. AND TANAKA, Y.: Cerebral ischemia model with conscious mice-Involvement of NMDA receptor activation and derangement of learning and memory ability. J. Pharmacol. Methods 23: 311-327, 1990.
30. HONEY, C. R., MILJKOVIC, Z. AND MACDONALD, J. F.: Ketamine and phencyclidine cause a voltage-dependent block of responses to I-aspartic acid. Neurosci. Lett. 61: 135-139, 1985.
31. JANSEN, K. L. R., FAULL, R. L. M., DRAGUNOW, M. AND SYNEK, B. L.: Alzheimer's disease - Changes in hippocampal N-methyl-d-aspartate, quisqualate, neurotensin, adenosine, benzodiazepine, serotonin and opioid receptors - An autoradiographic study. Neuroscience 39: 613-627, 1990.
32. JAVITT, D. C. AND ZUKIN, S. R.: Recent advances in the phencyclidine model of schizophrenia. Am. J. Psychiatry 148: 1301-1308, 1991.
33. 3H]TCP binding: Effects of glycine, magnesium, and N-methyl-d-aspartate agonists. Eur. J. Pharmacol. 152: 141-146, 1988.
34. KESNER, R. P. AND DAKIS, M.: Phencyclidine injections into the dorsal hippocampus disrupt long-but not short-term memory within a spatial learning task. Psychopharmacology 120: 203-208, 1995.
35. KESNER, R. P., HARDY, J. D. AND NOVAK, J. M.: Phencyclidine and behavior: II. Active avoidance learning and radial arm maze performance. Pharmacol. Biochem. Behav. 18: 351-356, 1983.
36. KIM, J. J., CLARK, R. E. AND THOMPSON, R. F.: Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. Behav. Neurosci. 109: 195-203, 1995.
37. KLEINSCHMIDT, A., BEAR, M. F. AND SINGER, W.: Blockade of "NMDA" receptors disrupts experience-dependent plasticity of kitten striate cortex. Science 238: 355-358, 1987.
38. LAROCHE, S., DOYERE, V. AND BLOCH, V.: Linear relationship between the magnitude of long-term potentiation in the dentate gyrus and associative learning in the rat: A demonstration using commissural and local infusion of an N-methyl-d-aspartate receptor antagonist. Neuroscience 28: 375-386, 1989.
39. LECCESE, A. P., MARQUIS, K. L., MATTIA, A. AND MORETON, J. E.: The anticonvulsant and behavioral effects of phencyclidine and ketamine following chronic treatment in rats. Behav. Brain Res. 22: 257-264, 1986.
40. MAJEWSKA, M. D., PARAMESWARAN, S., VU, T. AND LONDON, E. D.: Divergent ontogeny of sigma and phencyclidine binding sites in the rat brain. Dev. Brain Res. 47: 13-18, 1989.
41. MATTHIES, H.: In search of cellular mechanisms of memory. Prog. Neurobiol. 32: 277-349, 1989.
42. MCCANN, D. J. AND WINTER, J. C.: Effects of phencyclidine, N-allyl-N-normetazocine (SKF-10,047), and verapamil on performance in a radial maze. Pharmacol. Biochem. Behav. 24: 187-191, 1986.
43. MCCORMICK, D. A. AND THOMPSON, R. F.: Cerebellum: Essential involvement in the classically conditioned eyelid response. Science 223: 296-299, 1984.
44. MCINTOSH, T. K., VINK, R., SOARES, H., HAYES, R. AND SIMON, R.: Effect of noncompetitive blockade of N-methyl-d-aspartate receptors on the neurochemical sequelae of experimental brain injury. J. Neurochem. 55: 1170-1179, 1990.
45. MCLAMB, R. L., WILLIAMS, L. R., NANRY, K. P., WILSON, W. A. AND TILSON, H. A.: MK-801 impedes the acquisition of a spatial memory task in rats. Pharmacol. Biochem. Behav. 37: 41-45, 1990.
46. MELDRUM, B. S., MORONI, F., SIMON, R. P. AND WOODS, J. H., EDS.: Excitatory Amino Acids. Raven Press, New York, 1991.
47. 3H]-glutamate-binding sites in rat brain. J. Neurosci. 5: 2909-2919, 1985.
48. MONAHAN, J. B., HANDELMANN, G. E., HOOD, W. F. AND CORDI, A. A.: d-Cycloserine, a positive modulator of the N-methyl-d-aspartate receptor, enhances performance of learning tasks in rats. Pharmacol. Biochem. Behav. 34: 649-653, 1989.
49. MONYER, H., BURNASHEV, N., LAURIE, D. J., SAKMANN, B. AND SEEBURG, P. H.: Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12: 529-540, 1994.
50. MORRIS, R. G. M.: Parallel Distributed Processing: Implications for Psychology and Neurobiology. Clarendon Press, Oxford, 1989.
51. MORRIS, R. G. M., ANDERSON, E., LYNCH, G. S. AND BAUDRY, M.: Selective impairment of learning and blockade of long-term potentiation by an N-methyl-d-aspartate receptor antagonist, AP5. Nature 319: 774-776, 1986.
52. MORRIS, R. G. M., DAVIS, S. AND BUTCHER, S. P.: Hippocampal synaptic plasticity and NMDA receptors: A role in information storage? Phil. Trans. Roy. Soc. (Lond.) B 329: 187-204, 1990.
53. MOYER, J. R., JR., DEYO, R. A. AND DISTERHOFT, J. F.: Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behav. Neurosci. 104: 243-252, 1990.
54. NICHOLI, A. R.: The nontherapeutic use of psychoactive drugs. N. Engl. J. Med. 308: 925-933, 1983.
55. O'SHAUGHNESSY, C. T. AND LODGE, D.: N-methyl-d-aspartate receptor-mediated increase in intracellular calcium is reduced by ketamine and phencyclidine. Eur. J. Pharmacol. 153: 201-209, 1988.
56. OLNEY, J. W., LABRUYERE, J. AND PRICE, M. T.: Pathological changes induced in cerebrocortical neurons by phencyclidine and related drugs. Science 244: 1360-1362, 1989.
57. OLNEY, J. W.: Excitatory amino acids and neuropsychiatric disorders. Biol. Psychiatry 26: 505-525, 1990.
58. OLTON, D. S.: Memory functions and the hippocampus. In Neurobiology of the Hippocampus, ed. by W. Siefert, pp. 335-374, Academic, London, 1983.
59. PEARLSON, G. D.: Psychiatric and medical syndromes associated with phencyclidine (PCP) abuse. Johns Hopkins Med. J. 148: 25-33, 1981.
60. PERRETT, S. P., RUIZ, B. P. AND MAUK, M. D.: Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. J. Neurosci. 13: 1708-1718, 1993.
61. 3H]MK-801 binding in Alzheimer's disease. J. Neurochem. 53: 698-704, 1989.
62. RAWLINS, J. N. P.: Associations across time: The hippocampus as a temporary memory store. Behav. Brain Sci. 8: 479-496, 1985.
63. 3H]-labeled MK-801 binding to the excitatory amino acid receptor complex from rat brain is enhanced by glycine. Proc. Natl. Acad. Sci. U.S.A. 84: 7744-7748, 1987.
64. ROBINSON, G. B., PORT, R. L. AND STILLWELL, E. J.: Latent inhibition of the classically conditioned rabbit nictitating membrane response is unaffected by the NMDA antagonist MK801. Psychobiology 21: 120-124, 1993.
65. ROBINSON, G. B.: MK801 retards acquisition of a classically conditioned response without affecting conditioning-related alterations in perforant path-granule cell synaptic transmission. Psychobiology 21: 253-264, 1993.
66. ROBINSON, G. S., CROOKS, G. B., SHINKMAN, P. G. AND GALLAGHER, M.: Behavioural effects of MK-801 mimic deficits associated with hippocampal damage. Psychobiology 17: 156-164, 1989.
67. ROSENMUND, C., LEGENDRE, P. AND WESTBROOK, G. L.: Expression of NMDA channels on cerebellar Purkinje cells acutely dissociated from newborn rats. J. Neurophysiol. 68: 1901-1905, 1992.
68. SCAVIO, M. J., CLIFT, P. S. AND WILLS, J. C.: Posttraining effects of amphetamine, chlorpromazine, ketamine, and scopolamine on the acquisition and extinction of the rabbit's conditioned nictitating membrane response. Bebav. Neurosci. 106: 900-908, 1992.
69. SCHINDLER, C. W. AND HARVEY, J. A.: Use of classical conditioning procedures in behavioral pharmacology. Drug Dev. Res. 20: 169-187, 1990.
70. SCHMALTZ, L. W. AND THEIOS, J.: Acquisition and extinction of a classically conditioned reflex in hippocampectomized rabbits (Oryctolagus cuniculus). J. Comp. Physiol. Psychol. 79: 328-333, 1972.
71. SCHWARTZ, B. L., HASHTROUDI, S., HERTING, R. L., HANDERSON, H. AND DEUTSCH, S. I.: Glycine prodrug facilitates memory retrieval in humans. Neurology 41: 1341-1343, 1991.
72. SEKIGUCHI, M., OKAMOTO, K. AND SAKAI, Y.: NMDA-receptors on Purkinje cell dendrites in guinea pig cerebellar slices. Brain Res. 437: 402-406, 1987.
73. SHAPIRO, M. L. AND CARAMANOS, Z.: NMDA antagonist MK-801 impairs acquisition but not performance of spatial working and reference memory. Psychobiology 18: 231-243, 1990.
74. SHOWALTER, C. V. AND THORNTON, W. E.: Clinical pharmacology of phencyclidine toxicity. Am. J. Psychiat. 134: 1234-1238, 1977.
75. SINGH, L., OLES, R. J. AND TRICKLEBANK, M. D.: Modulation of seizure susceptibility in the mouse by the strychnine-insensitive glycine recognition site of the NMDA receptor ion channel complex. Br. J. Pharmacol. 99: 285-288, 1990.
76. SOLOMON, P. R.: Role of the hippocampus in blocking and conditioned inhibition of the rabbit's nictitating membrane response. J. Comp. Physiol. Psychol. 91: 407-417, 1977.
77. SOLOMON, P. R.: Temporal versus spatial information processing theories of hippocampal function. Psych. Bull. 86: 1272-1279, 1979.
78. SOLOMON, P. R., BEAL, M. F. AND PENDLEBURY, W. W.: Age-related disruption of classical conditioning: A model systems approach to memory disorders. Neurobiol. Aging 9: 535-546, 1988.
79. SOLOMON, P. R. AND GROCCIA-ELLISON, M. E.: Classic conditioning in aged rabbits: Delay, trace, and long-delay conditioning. Behav. Neurosci. 110: 427-435, 1996
80. SOLOMON, P. R. AND MOORE, J. W.: Latent inhibition and stimulus generalization of the classically conditioned nictitating membrane response in rabbits (Oryctolagus cuniculus) following dorsal hippocampal ablation. J. Comp. Physiol. Psychol. 89: 1192-1203, 1975.
81. SOLOMON, P. R., SOLOMON, S. D., VANDER SCHAAF, E. V. AND PERRY, H. E.: Altered activity in the hippocampus is more detrimental to classical conditioning than removing the structure. Science 220: 329-331, 1983.
82. SOLOMON, P. R., VANDER SCHAAF, E. V., THOMPSON, R. F. AND WEISZ, D. J.: Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behav. Neurosci. 100: 729-744, 1986.
83. SQUIRE, L.: Memory and Brain. Oxford, New York, 1987.
84. STAUBLI, U., THIBAULT, O., DILORENZO, M. AND LYNCH, G. S.: Antagonism of NMDA receptors impairs acquisition but not retention of olfactory memory. Behav. Neurosci. 103: 54-60, 1989.
85. STRINGER, J. L. AND GUYENET, P. G.: Effect of phencyclidines on hippocampal pyramidal cells. Brain Res. 252: 343-352, 1982.
86. STRINGER, J. L. AND GUYENET, P. G.: Elimination of long-term potentiation in the hippocampus by phencyclidine and ketamine. Brain Res. 258: 159-164, 1983.
87. THOMPSON, L. T., AKASE, E., MOYER, J. R., JR. AND DISTERHOFT, J. F.: A system for quantitative analysis of associative learning: 1. Hardware interfaces with cross-species applications. J. Neurosci. Methods 54: 109-117; 1994.
88. THOMPSON, L. T., MOSKAL, J. R. AND DISTERHOFT, J. F.: Hippocampus-dependent learning facilitated by a monoclonal antibody or d-cycloserine. Nature 359: 638-641, 1992.
89. THOMPSON, L. T., MOYER, J. R., JR. AND DISTERHOFT, J. F.: Trace eyeblink conditioning in rabbits demonstrates heterogeneity of learning ability both between and within age groups. Neurobiol. Aging 17: 619-629, 1996a.
90. THOMPSON, L. T., MOYER, J. R., JR. AND DISTERHOFT, J. F.: Transient changes in excitability of rabbit CA3 neurons with a time-course appropriate to support memory consolidation. J. Neurophysiol. 76: 1836-1849, 1996b.
91. THOMPSON, R. F.: The neurobiology of learning and memory. Science 233: 941-947, 1986.
92. THOMPSON, R. F.: Classical conditioning: The Rosetta stone for brain substrates of age related deficits in learning and memory. Neurobiol. Aging 9: 547-548, 1988.
93. THOMPSON, R. F.: Neural mechanisms of classical conditioning in mammals. Phil. Trans. Roy. Soc. (Lond.) B 329: 161-170, 1990.
94. THOMPSON, R. F.: Are memory traces localized or distributed? Neuropsychology 29: 571-582, 1991.
95. THOMPSON, R. F., BERGER, T. W., CEGAVSKE, C. F., PATTERSON, M. M., ROEMER, R. A., TEYLER, T. A. AND YOUNG, R. A.: The search for the engram. Am. Psychol. 31: 209-227, 1976.
96. VINCENT, J. P., KARTALOVSKI, B., GENEST, P., KAMENKA, J. M. AND LAZDUNSKI, M.: Interaction of phencyclidine ("angel dust") with specific receptor in rat brain membranes. Proc. Nat. Acad. Sci. U.S.A. 76: 4678-4682, 1979.
97. WARD, L., MASON, S. E. AND ABRAHAM, W. C.: Effects of the NMDA antagonists CPP and MK-801 on radial arm maze performance in rats. Pharmacol. Biochem. Behav. 35: 785-790, 1990.
98. WATKINS, J. C. AND COLLINGRIDGE, G. L.: The NMDA Receptor. IRL Press, Oxford, 1989.
99. WHISHAW, I. Q. AND AUER, R. N.: Immediate and long-lasting effects of MK-801 on motor activity, spatial navigation in a swimming pool and EEG in the rat. Psychopharmacology 98: 500-507, 1989.
100. 3H]MK-801 labels a site on the N-methyl-d-aspartate receptor channel complex in rat brain membrane. J. Neurochem. 50: 274-281, 1988.
101. WOODRUFF-PAK, D. S., LAVOND, D. G. AND THOMPSON, R. F.: Trace conditioning: Abolished by cerebellar nuclear lesions but not lateral cerebellar cortex aspirations. Brain Res. 348: 249-260, 1985.
102. YI, S., SNELL, L. D. AND JOHNSON, K. M.: Linkage between phencyclidine (PCP) and N-methyl-d-aspartate (NMDA) receptors in the cerebellum. Brain Res. 445: 147-151, 1988.
103. 3H]phencyclidine binding in rat brain central nervous system. Proc. Natl. Acad. Sci. U.S.A. 76: 5372-5376, 1979.