Ketamine-induced NMDA receptor hypofunction as a model of memory impairment and psychosis

Neuropsychopharmacology

Volumn 20, Issue 2, 1999, Pages 106-118

  Newcomer, John W ^a,b   Farber, Nuri B ^a   Jevtovic Todorovic, Vesna ^a   Selke, Gregg ^a   Melson, Angela Kelly ^a   Hershey, Tamara ^a   Craft, Suzanne ^c,d   Olney, John W ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Cognition; Glutamate; Ketamine; Memory; NMDA; Schizophrenia

Indexed keywords

KETAMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ADULT; AMNESIA; ARTICLE; BEHAVIOR; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DOSE RESPONSE; DOUBLE BLIND PROCEDURE; DRUG BLOOD LEVEL; HUMAN; HUMAN EXPERIMENT; INTRAVENOUS DRUG ADMINISTRATION; MALE; MODEL; NEGATIVE SYNDROME; NORMAL HUMAN; PRIORITY JOURNAL; PSYCHOSIS; RANDOMIZED CONTROLLED TRIAL; SCHIZOPHRENIA; TECHNIQUE;

ADULT; ANIMALS; COGNITION; DEPRESSION, CHEMICAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DOUBLE-BLIND METHOD; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; HUMANS; INJECTIONS, INTRAVENOUS; KETAMINE; MALE; MEMORY DISORDERS; MENTAL RECALL; PSYCHOSES, SUBSTANCE-INDUCED; RATS; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 0033080733     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0893-133X(98)00067-0     Document Type: Article

References (109)

1. Aggleton J.P., Nicol R.M., Huston A.E., Fairbairn A.F. The performance of amnesic subjects on tests of experimental amnesia in animals. Delayed matching-to-sample and concurrent learning Neuropsychologia. 26(2):1988;265-272.
2. Alvarez P., Zola-Morgan S., Squire L.R. The animal model of human amnesia. Long-term memory impaired and short-term memory intact Proc Natl Acad Sci USA. 91:1994;5637-5641.
3. Andreasen N.C. Negative symptoms in schizophrenia. definition and reliability Arch Gen Psychiatry. 39:1982;784-788.
4. Backer-Cave C., Squire L.R. Intact verbal and nonverbal short-term memory following damage to the human hippocampus. Hippocampus. 2(2):1992;151-164.
5. Bakker C.B., Amini F.B. Observations on the psychotomimetic effects of Sernyl. Compr Psychiatry. 2:1961;269-280.
6. Balster R.L., Chait L.D. The behavioral pharmacology of phencyclidine. Clin Toxicol. 9:1976;513-528.
7. Bliss T.V.P., Collingridge G.L. A synaptic model of memory. Long-term potentiation in the hippocampus Nature. 361(6407):1993;31-39.
8. Buffalo E.A., Gillam M.P., Allen R.R., Paule M.G. Acute behavioral effects of MK-801 in rhesus monkeys. Assessment using an operant test battery Pharmacol Biochem Behav. 48(4):1994;935-940.
9. Butelman E.R. A novel NMDA antagonist, MK-801, impairs performance in a hippocampal-dependent spatial learning task. Pharmacol Biochem Behav. 34:1989;13-16.
10. Butters N., Sax D., Montgomery K., Tarlow S. Comparison of the neuropsychological deficits associated with early and advanced Huntington's disease. Arch Neurol. 35:1978;585-589.
11. Cannon T.D., Zorrilla L.E., Shtasel D., Gur R.E., Gur R.C., Marco E.J., Moberg P., Price R.A. Neuropsychological functioning in siblings discordant for schizophrenia and healthy volunteers. Arch Gen Psychiatry. 51:1994;651.
12. Clarke R.S.J., Bali I.M., Issac M., Dundee J.W., Sheridan B. Plasma cortisol and blood sugar following minor surgery under intravenous anaesthetics. Anaesthesia. 29:1974;545-550.
13. Cohen B.D., Rosenbaum G., Luby E.D., Gottlieb J.S. Comparison of phencyclidine hydrochloride (Sernyl) with other drugs. Arch Gen Psychiatry. 6:1962;395-401.
14. Collingridge G.L., Bliss T.V.P. Memories of NMDA receptors and LTP. Trends Neurosci. 18(2):1995;54-56.
15. Corssen G., Domino E.F. Dissociative anesthesia. Further pharmacologic studies and first clinical experience with the phencyclidine derivative CI-581 Anesth Analg. 45:1966;29-40.
16. Craft S., Dagogo-Jack S.E., Wiethop B.V., Murphy C., Nevins R.T., Fleischman S., Rice V., Newcomer J.W., Cryer P.I. The effects of hyperglycemia on memory and hormone levels in dementia of the Alzheimer type. A longitudinal study Behav Neurosci. 107(6):1993;926-940.
17. Craft S., Newcomer J.W., Kanne S., Dagogo-Jack S., Cryer P., Sheline Y., Luby J., Dagogo-Jack A., Alderson A. Memory improvement following induced hyperinsulinemia in Alzheimer's Disease. Neurobiol Aging. 17:1996;123-130.
18. Crooks E.B., Robinson G.S., Hatfield T.J., Graham P.W., Gallagher M. Intraventricular administration of the NMDA antagonist APV disrupts learning of an odour aversion that is potentiated by taste. Soc Neurosci Abstr. 15:1989;464.
19. Danysz W., Wroblewski J.T., Costa E. Learning impairment in rats by N-methyl-D-aspartate receptor antagonists. Neuropharmacology. 27:1988;653-656.
20. Davies B.M., Beech H.L. The effect of 1-arylcyclohexylamine (Sernyl) on twelve normal volunteers. J Ment Sci. 106:1960;912-924.
21. Davis S., Butcher S.P., Morris R.G.M. 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. J Neurosci. 12(1):1992;21-34.
22. Deutsch S.I., Mastropaolo J., Schwartz B.L., Rosse R.B., Morihisa J.M. A "glutamatergic hypothesis" of schizophrenia. Rationale for pharmacotherapy with glycine. Clin Neuropharmacol. 12(1):1989;1-13.
23. Domino E, Luby E (1981): Abnormal mental states induced by phencyclidine as a model of schizophrenia. In Domino E (ed), PCP (Phencyclidine): Historical and Current Perspectives, Ann Arbor, NPP Books, pp 401-418.
24. Doyere V., Laroche S. Linear relationship between the maintenance of hippocampal long-term potentiation and retention of an associative memory. Hippocampus. 2(1):1992;39-48.
25. Erard R., Luisada P.V., Peele R. The PCP psychosis. Prolonged intoxication or drug-precipitated functional illness? J Psychedelic Drugs. 12:1980;235-245.
26. Fahringer E.E., Foley E.L., Redgate E.S. Pituitary adrenal response to ketamine and the inhibition of the response by catecholaminergic blockade. Neuroendocrinology. 14:1974;151-164.
27. Farmer R., Pierce C. Plasma cortisol determination. Radioimmunoassay and competitive binding compared Clin Chem. 20:1974;411-414.
28. Frederick D.L., Gillam M.P., Allen R.R., Paule M.G. Acute behavioral effects of phencyclidine on rhesus monkey performance in an operant test battery. Pharmacol Biochem Behav. 52(4):1995;789-797.
29. Funahashi S., Bruce C.J., Goldman-Rakic P.S. Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J Neurophysiol. 61(2):1989;331-349.
30. Gangarosa M.E., Saykin A.J., Malamut B.L., Gur R.C. New scoring systems for the Wechsler Memory Scale. Interrater reliability J Clin Exp Neuropsychol. 10:1988;1-43.
31. Ghoneim M.M., Hinrichs J.V., Mewaldt S.P., Petersen R.C. Ketamine. Behavioral effects of subanesthetic doses J Clin Psychopharmacol. 5(2):1985;70-77.
32. Golden C.J. Stroop Color and Word Test. A Manual for Clinical and Experimental Uses:1978;Stoelting Co, Chicago.
33. Goodman Gillman A., Rall T.W., Nies A.S., Taylor P. The Pharmacological Basis of Therapeutics. 8:1990;Pergamon Press, New York. Inc.
34. Green M.F. What are the functional consequences of neurocognitive deficits in schizophrenia? Am J Psychiatry. 153:1996;321-330.
35. Gruzelier J., Seymour K., Wilson J. Impairments on neuropsychologic tests of temporohippocampal and frontohippocampal functions and word fluency in remitting schizophrenic and affective disorders. Arch Gen Psychiatry. 45:1988;623-629.
36. Handelman G.E., Contreras P.C., O'Donohue T.L. Selective memory impairment by phencyclidine in rats. Eur J Pharmacol. 140:1987;69-73.
37. Harris J.A., Biersner R.J., Edwards D., Bailey L.W. Attention, learning, and personality during ketamine emergence. A pilot study Anesth Analg. 54(2):1975;169-172.
38. Hedlund J.L., Vieweg B.W. The Brief Psychiatry Rating Scale (BPRS). A comprehensive review J Oper Psychiatry. 11:1980;48-64.
39. Hershey T., Craft S., Glauser T.A., Hale S. Short-term and long-term memory in early temporal lobe dysfunction. Neuropsychology. 12(1):1998;52-64.
40. Izumi Y., Clifford D.B., Zorumski C.F. Glucose metabolism and hippocampal long-term potentiation. Soc Neurosci Abstr. 19:1993;911.
41. Javitt D.C., Zukin S.R. Recent advances in the phencyclidine model of schizophrenia. Am J Psychiatry. 148(10):1991;1301-1308.
42. Johnstone M., Evans V., Baigel S. Sernyl (CI-395) in clinical anaesthesia. Br J Anaesth. 31:1959;433-439.
43. Jones K.W., Bauerle L., DeNoble V. Differential effects of sigma and phencyclidine receptor ligands on learning. Eur J Pharmacol. 179:1990;97-102.
44. Kaniaris P., Lekakis D., Kykoniatis M., Kastanas E. Serum free fatty acid and blood sugar levels in children under halothane, thiopentone, and ketamine anaesthesia. Can Anaesth Soc J. 22:1975;509-518.
45. Kim J.S., Kornhuber H.H., Holzmuller B., Schmid-Burgk W., Mergner T., Krzepinski G. Reduction of cerebral spinal fluid glutamic acid in Huntington's chorea and in schizophrenic patients. Arch Psychiatry Nervenkr. 228:1980;7-10. b.
46. Kim J.S., Kornhuber H.H., Schmid-Burgk W., Holzmuller B. Low cerebrospinal fluid glutamate in schizophrenic patients and a new hypothesis on schizophrenia. Neurosci Lett. 20:1980;379-382. a.
47. Kowalska D.M. Effects of hippocampal lesions on spatial delayed responses in dog. Hippocampus. 5:1995;363-370.
48. Krystal J.H., Karper L.P., Seibyl J.P., Freeman G.K., Delaney R., Bremner J.D., Heninger G.R., Bowers M.B., Charney D.S. Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans. Arch Gen Psychiatry. 51:1994;199-214.
49. Kuzuya H., Blix P., Horwitz D., Steiner D., Rubenstein A. Determination of free and total insulin and C-peptide in insulin-treated diabetics. Diabetes. 26:1977;22-29.
50. Lahti A.C., Holcomb H.H., Medoff D.R., Tamminga C.A. Ketamine activates psychosis and alters limbic blood flow in schizophrenia. NeuroReport. 6:1995;869-872. a.
51. Lahti A.C., Koffel B., LaPorte D., Tamminga C.A. Subanesthetic doses of ketamine stimulate psychosis in schizophrenia. Neuropsychopharmacology. 13(1):1995;9-19. b.
52. Lodge D., Anis N.A. Effects of phencyclidine on excitatory amino acid activation of spinal interneurons in the cat. Eur J Pharmacol. 77:1982;203-204.
53. Lodge D., Aram J.A., Church J., Davies S.N., Martin D., O'Shaughnessy C.T., Zeman S. Excitatory amino acids and Phencyclidine-like drugs. Hicks T.P., Lodge D., McLennan H. Excitatory Amino Acid Transmission, New York, Alan R. 1987;83-90 Inc, Liss.
54. Luby E.D., Cohen B.D., Rosenbaum G., Gottlieb J.S., Kelley R. Study of a new schizophrenomimetic drug - sernyl. Arch Neuro Psychiatry. 81:1959;363-369.
55. Luby E.D., Gottlieb J.S., Cohen B.D., Rosenbaum G., Domino E.F. Model psychoses and schizophrenia. Am J Psychiatry. 119:1962;61-67.
56. Luciana M., Depue R.A., Arbisi P., Leon A. Facilitation of working memory in humans by a D2 dopamine receptor agonist. J Cog Neurosci. 4(1):1992;58-68.
57. Malhotra A.K., Pinals D.A., Adler C.M., Elman I., Clifton A., Pickar D., Breier A. Ketamine-induced exacerbation of psychotic symptoms and cognitive impairment in neuroleptic-free schizophrenics. Neuropsychopharmacology. 17(3):1997;141-150.
58. Malhotra A.K., Pinals D.A., Weingartner H., Sirocco K., Missar C.D., Picker D., Berier A. NMDA receptor function and human cognition. The effects of ketamine in healthy volunteers Neuropsychopharmacology. 14:1996;301-307.
59. McLamb R.L., Williams L.R., Nanary K.P., Wilson W.A., Tilson H.A. MK-801 impedes the acquisition of a spatial memory in rats. Pharmacol Biochem Behav. 37:1990;41-45.
60. McNamara R.K., Skelton R.W. The neuropharmacological and neurochemical basis of place learning in the Morris water maze. Brain Res Rev. 18:1993;33-49.
61. Milner B. Some effects of frontal lobectomy in man. Warren J.M., Akert K. The Frontal Granular Cortex and Behavior. 1964;McGraw-Hill, New York.
62. Mondadori C., Weiskrantz L., Buerki H., Petschke F., Fagg G.E. NMDA receptor antagonists can enhance or impair learning performance in animals. Exp Brain Res. 75:1989;449-456.
63. Morris R.G.M. 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 J Neurosci. 9(9):1989;3040-3057.
64. Morris R.G.M., Anderson E., Lynch G.S., Baudry M. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature. 319(6056):1986;774-776.
65. Morris R.G.M., Davis S., Butcher S.P. Hippocampal synaptic plasticity and NMDA receptors. A role in information storage? Phil Trans R Soc. 329(1253):1990;187-204.
66. Nestor P.G., Shenton M.E., McCarley R.W., Haimson J., Smith R.S., O'Donnell B., Kimble M., Kikinis R., Jolesz F.A. Neuropsychological correlates of MRI temporal lobe abnormalities in schizophrenia. Am J Psychiatry. 150:1993;1849-1855.
67. Newcomer J.W., Craft S., Fucetola R., Moldin S.O., Paras L., Selke G. Increase in declarative memory performance during controlled hyperglycemia in patients with schizophrenia. Soc Neurosci Abstr. 20(1):1994;810. a.
68. Newcomer JW, Craft S, Fucetola R, Moldin SO, Selke G, Paras L, Miller R (in press): Glucose-induced increase in memory performance in patients with schizophrenia. Schizophr Bull.
69. Newcomer J.W., Craft S., Hershey T., Askins K., Bardgett M.E. Glucocorticoid-induced impairment in declarative memory performance in adult humans. J Neurosci. 14(4):1994;2047-2053. b.
70. Nurnberger J.I., Blehar M., Kaufmann C.A., York-Cooler C., Simpson S., Harkavy-Friedman J. Diagnostic Interview for Genetic Studies. Rationale, Unique Features, Training Arch Gen Psychiatry. 51:1994;849-859.
71. Oldfield R.C. The assessment and analysis of handedness. The Edinburgh Inventory Neuropsychologia. 9:1971;97-113.
72. Olney J.W. Endogenous Excitotoxins and Neuropathological Disorders. Lodge D. Excitatory Amino Acids in Health and Disease. 1988;337-351 England, John Wiley & Sons Ltd, London. a.
73. Olney JW (1988b): Excitatory Transmitters and Neuropsychiatric Disorders. In Ferrendelli JA, Collins RC, Johnson EM (eds), Neurobiology of Amino Acids, Peptides, and Trophic Factors. Kluwer Academic Pub, pp 51-61.
74. Olney J.W., Farber N.B. Glutamate receptor dysfunction and schizophrenia. Arch Gen Psychiatry. 52:1995;998-1024.
75. Olney J.W., Labruyere J., Price M.T. Pathological changes induced in cerebrocortical neurons by phencyclidine and related drugs. Science. 244:1989;1360-1362.
76. Overall J.E. A brief psychiatric rating scale in psychopharmacology research. Pichot P. Psychological Measurements in Psychopharmacology, Modern Problems in Pharmacopsychiatry, Vol 7. 1974;67-78 Karger, Basel.
77. Oyama T., Matsumoto F., Kudo T. Effects of ketamine on adrenocortical function in man. Anesth Analg (Cleve). 49:1970;697-700.
78. Pandit K.S., Dundee J.W., Bovill J.G. Clinical studies of induction agents XXXVII. Amnesic action of ketamine Br J Anaesth. 43:1971;362-364.
79. Parada-Turska J., Turski W.A. Excitatory amino acid antagonists and memory. Effect of drugs acting at N-methyl-D-aspartate receptors in learning and memory tasks Neuropharmacol. 29(2):1990;1111-1116.
80. Pontecorvo M.J., Clissold D.B., White M.F., Ferkany J.W. N-methyl-D-aspartate antagonists and working memory performance. Comparison with the effects of scopolamine, propranolol, diazepam, and phenylisopropyladenosine Behav Neurosci. 105(4):1991;521-535.
81. Rains G.D., Milner B. Right-hippocampal contralateral-hand effect in the recall of spatial location in the tactual modality. Neuropsychologia. 32(10):1994;1233-1242.
82. Reich D.L., Silvay G. Ketamine. An update on the first twenty-years of clinical experience Can J Anaesth. 36(2):1989;186-197.
83. Rosenbaum G., Cohen B.D., Luby E.D., Gottlieb J.S., Yelen D. Comparison of Sernyl with other drugs. Simulation of schizophrenic performance with Sernyl, LSD-25, and Amobarbital (Amytal); I. attention, motor function, and proprioception Arch Gen Psychiatry. 1:1959;651-656.
84. Russell E.W. A multiple scoring method for assessment of complex memory functions. J Consult Clin Psychol. 43:1975;800-809.
85. Sakimura K., Kutsuwada T., Ito I., Manabe T., Takayama C., Kushiya E., Yagi T., Aizawa S., Inoue Y., Sugiyama H., Mishina M. Reduced hippocampal LTP and spatial learning in mice lacking NMDA receptor epsilon 1 subunit. Nature (Lett). 373:1995;151-155.
86. Saykin A.J., Gur R.C., Gur R.E., Mozley P.D., Mozley L.H., Resnick S.M., Kester D.B., Stafiniak P. Neuropsychological function in schizophrenia. Selective impairment in memory and learning Arch Gen Psychiatry. 48:1991;618-624.
87. Saykin A.J., Shtasel D.L., Gur R.E., Kester D.B., Mozley L.H., Stafiniak P., Gur R.C. Neuropsychological deficits in neuroleptic naive patients with first-episode schizophrenia. Arch Gen Psychiatry. 51:1994;124.
88. Shah S.D., Clutter W.E., Cryer P.E. External and internal standards in the single isotope derivative (radioenzymatic) assay of plasma norepinephrine and epinephrine in normal humans and patients with diabetes mellitus or chronic renal failure. J Lab Clin Med. 106:1985;624-629.
89. Sherman A.D., Davidson A.T., Baruah S., Hegwood T.S., Waziri R. Evidence of glutamatergic deficiency in schizophrenia. Neurosci Lett. 121:1991;77-80.
90. Sidman M., Stoddard L.T., Mohr J.P. Some additional quantitative observations of immediate memory in a patient with bilateral hippocampal lesions. Neuropsychologia. 6:1968;245-254.
91. Spangler E.L., Bresnahan E.L., Garofalo P., Muth N.J., Heller B., Ingram D.K. NMDA receptor channel antagonism by dizocilpine (MK-801) impairs performance of rats in aversively motivated complex maze tasks. Pharmacol Biochem Behav. 40(4):1991;949-958.
92. Squire L.R., Zola-Morgan S., Chen K.S. Human amnesia and animal models of amnesia. Performance of amnesic patients on tests designed for the monkey Behav Neurosci. 102(2):1988;210-221.
93. Squire LR (1987): Memory and Brain, New York, Oxford University Press.
94. Storandt M., Botwinick J., Danziger W.L., Berg L., Hughes C.P. Psychometric differentiation of mild senile dementia of the Alzheimer type. Arch Neurol. 41:1984;497-499.
95. Thompson D.M., Moerschbaecher J.M. Phencyclidine in combination with d-amphetamine. differential effects on acquisition and performance of response chains in monkeys Pharmacol Biochem Behav. 20:1984;619-627.
96. Thompson D.M., Winsauer P.J., Mastropaolo J. Effects of phencyclidine, ketamine and MDMA on complex operant behavior in monkeys. Pharmacol Biochem Behav. 26:1987;401-405.
97. Tonkiss J., Morris R.G.M., Rawlins J.N.P. Intra-ventricular infusion of the NMDA antagonist AP5 impairs performance on a non-spatial operant DRL task in the rat. Exp Brain Res. 73:1988;181-188.
98. Tsai G., Passani L.A., Slusher B.S., Carter R., Baer L., Kleinman J.E., Coyle J.T. Abnormal excitatory neurotransmitter metabolism in schizophrenic brains. Arch Gen Psychiatry. 52:1995;829-836.
99. Vincent J.P., Kartalovski B., Geneste P., Kamenka J.M., Lazdunski M. Interaction of phencyclidine ("angel dust") with a specific receptor in rat brain membranes. Proc Natl Acad Sci USA. 76:1979;4678-4682.
100. Walker D.L., Gold P.E. Effects of the novel NMDA antagonist, NPC 12626, on long-term potentiation, learning and memory. Brain Res. 549(2):1991;213-221.
101. Ward L., Mason S.E., Abraham W.C. Effects of the NMDA antagonists, CPP and MK-801 on the radial arm maze performance in rats. Pharmacol Biochem Behav. 35:1990;785-790.
102. Wechsler D. A standardized memory scale for clinical use. J Psychol. 19:1945;87-95.
103. Wechsler D (1987): Wechsler Memory Scale - Revised. New York, Harcourt Brace Jovanovich.
104. White P.F., Way W.L., Trevor A.J. Ketamine - Its pharmacology and therapeutic uses. Anesthesiology. 56:1982;119-136.
105. Winocur G. Effects of interference on discrimination and learning and recall by rats with hippocampal lesions. Physiol Behav. 22:1978;339-345.
106. Yesavage J.A., Freeman A.M. III Acute phencyclidine (PCP) intoxication. Psychopathology and prognosis J Clin Psychiatry. 44:1978;664-665.
107. Zola-Morgan S., Squire L.R. Medial temporal lesions in monkeys impair memory on a variety of tasks sensitive to human amnesia. Behav Neurosci. 99:1985;22-34.
108. Zsigmond EK, Domino EF (1990): Clinical pharmacology of ketamine. In EF Domino (ed), Status of Ketamine in Anesthesiology. Ann Arbor, NPP Books, pp 27-76.
109. 3H]phencyclidine binding in rat central nervous system. Proc Natl Acad Sci USA. 76:1979;5372-5376.