Acute and long-term effects of MK-801 on direct cortical input evoked homosynaptic and heterosynaptic plasticity in the CA1 region of the female rat

European Journal of Neuroscience

Volumn 26, Issue 10, 2007, Pages 2873-2883

  Wöhrl, Robert ^a   Eisenach, Sven ^a   Manahan Vaughan, Denise ^b   Heinemann, Uwe ^a   Von Haebler, Dorothea ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

CA1; Direct cortical input; Long term potentiation; MK 801 induced psychosis; Neuronal degeneration; NMDA receptor

Indexed keywords

DIZOCILPINE; PHENCYCLIDINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATAXIA; BEHAVIOR CHANGE; BRAIN DEPTH STIMULATION; COGNITION; CONTROLLED STUDY; DEPRESSION; EVOKED CORTICAL RESPONSE; EVOKED RESPONSE; FEMALE; HIPPOCAMPUS; HISTOLOGY; LONG TERM POTENTIATION; MORPHOLOGY; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PSYCHOSIS; RAT; SYNAPTIC MEMBRANE;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; DIZOCILPINE MALEATE; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; HIPPOCAMPUS; NEURONAL PLASTICITY; NEURONS; RATS; RATS, WISTAR; SYNAPSES; TIME FACTORS;

EID: 36148955108     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05899.x     Document Type: Article

References (75)

1. Amaral, D.G. Witter, M.P. (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience, 31, 571 591.
2. Andine, P., Widermark, N., Axelsson, R., Nyberg, G., Olofsson, U., Martensson, E. Sandberg, M. (1999) Characterization of MK-801-induced behavior as a putative rat model of psychosis. J. Pharmacol. Exp. Ther., 290, 1393 1408.
3. Anis, N.A., Berry, S.C., Burton, N.R. Lodge, D. (1983) The dissociative anaesthetics, ketamine and phencyclidine, selectively reduce excitation of central mammalian neurones by N-methyl-aspartate. Br. J. Pharmacol., 79, 565 575.
4. Auer, R.N. (1996) Effect of age and sex on N-methyl-D-aspartate antagonist-induced neuronal necrosis in rats. Stroke, 27, 743 746.
5. Bernstein, H.G., Braunewell, K.H., Spilker, C., Danos, P., Baumann, B., Funke, S., Diekmann, S., Gundelfinger, E.D. Bogerts, B. (2002) Hippocampal expression of the calcium sensor protein visinin-like protein-1 in schizophrenia. Neuroreport, 13, 393 396.
6. Bernstein, H.G., Becker, A., Keilhoff, G., Spilker, C., Gorczyca, W.A., Braunewell, K.H. Grecksch, G. (2003) Brain region-specific changes in the expression of calcium sensor proteins after repeated applications of ketamine to rats. Neurosci. Lett., 339, 95 98.
7. Bliss, T.V. Collingridge, G.L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature, 361, 31 39.
8. Boulton, C.L., von Haebler, D. Heinemann, U. (1992) Tracing of axonal connections by rhodamine-dextran-amine in the rat hippocampal-entorhinal cortex slice preparation. Hippocampus, 2, 99 106.
9. Brun, V.H., Otnass, M.K., Molden, S., Steffenach, H.A., Witter, M.P., Moser, M.B. Moser, E.I. (2002) Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science, 296, 2243 2246.
10. Buck, N., Cali, S. Behr, J. (2006) Enhancement of long-term potentiation at CA1-subiculum synapses in MK-801-treated rats. Neurosci. Lett., 392, 5 9.
11. Bueno, A., De Olmos, S., Heimer, L. De Olmos, J. (2003a) NMDA-antagonist MK-801-induced neuronal degeneration in Wistar rat brain detected by the amino-cupric-silver method. Exp. Toxicol. Pathol., 54, 319 334.
12. Bueno, A., De Olmos S., Manzini, F., de Desmond, N.L. De Olmos J. (2003b) Strain and colony differences in the neurotoxic sequelae of MK-801 visualized with the amino-cupric-silver method. Exp Toxicol. Pathol, 55, 287 294.
13. Cohen, G.M. (1997) Caspases: the executioners of apoptosis. Biochem. J., 326, 1 16.
14. Colbert, C.M. Levy, W.B. (1992) Electrophysiological and pharmacological characterization of perforant path synapses in CA1: mediation by glutamate receptors. J. Neurophysiol., 68, 1 8.
15. Colbert, C.M. Levy, W.B. (1993) Long-term potentiation of perforant path synapses in hippocampal CA1 in vitro. Brain Res., 606, 87 91.
16. Davies, S.N., Martin, D., Millar, J.D., Aram, J.A., Church, J. Lodge, D. (1988) Differences in results from in vivo and in vitro studies on the use-dependency of N-methylaspartate antagonism by MK-801 and other phencyclidine receptor ligands. Eur. J. Pharmacol., 145, 141 151.
17. D'Souza, D.N., Harlan, R.E. Garcia, M.M. (2002) Sexually dimorphic effects of morphine and MK-801: sex steroid-dependent and -independent mechanisms. J. Appl. Physiol., 92, 493 503.
18. Doller, H.J. Weight, F.F. (1985) Perforant pathway-evoked long-term potentiation of CA1 neurons in the hippocampal slice preparation. Brain Res., 333, 305 310.
19. Dudek, S.M. Bear, M.F. (1992) Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc. Natl Acad. Sci. USA, 89, 4363 4367.
20. Dugladze, T., Lepsveridze, E., Breustedt, J., Kehrer, C., Heinemann, U. Gloveli, T. (2004) Effects of phencyclidines on signal transfer from the entorhinal cortex to the hippocampus in rats. Neurosci. Lett., 354, 185 188.
21. Dvorak-Carbone, H. Schuman, E.M. (1999a) Long-term depression of temporoammonic-CA1 hippocampal synaptic transmission. J. Neurophysiol., 81, 1036 1044.
22. Dvorak-Carbone, H. Schuman, E.M. (1999b) Patterned activity in stratum lacunosum moleculare inhibits CA1 pyramidal neuron firing. J. Neurophysiol., 82, 3213 3222.
23. Empson, R.M. Heinemann, U. (1995) Perforant path connections to area CA1 are predominantly inhibitory in the rat hippocampal-entorhinal cortex combined slice preparation. Hippocampus, 5, 104 107.
24. Erchova, I., Kreck, G., Heinemann, U. Herz, A.V. (2004) Dynamics of rat entorhinal cortex layer II and III cells: characteristics of membrane potential resonance at rest predict oscillation properties near threshold. J. Physiol., 560, 89 110.
25. Farber, N.B., Wozniak, D.F., Price, M.T., Labruyere, J., Huss, J., St Peter, H. Olney, J.W. (1995) Age-specific neurotoxicity in the rat associated with NMDA receptor blockade: potential relevance to schizophrenia? Biol. Psychiatry, 38, 788 796.
26. Farber, N.B., Kim, S.H., Dikranian, K., Jiang, X.P. Heinkel, C. (2002) Receptor mechanisms and circuitry underlying NMDA antagonist neurotoxicity. Mol. Psychiatry, 7, 32 43.
27. Fix, A.S. (1994) Pathological effects of MK-801 in the rat posterior cingulate/retrosplenial cortex. Psychopharmacol. Bull., 30, 577 583.
28. Fix, A.S., Olney, J.W. Wozniak, D.F. (1994) Pathomorphologic effects of NMDA antagonists in the rat posterior cingulate/retrosplenial cerebral cortex: a review. Drug Dev. Res., 32, 147 152.
29. Fix, A.S., Wozniak, D.F., Truex, L.L., McEwen, M., Miller, J.P. Olney, J.W. (1995) Quantitative analysis of factors influencing neuronal necrosis induced by MK-801 in the rat posterior cingulate/retrosplenial cortex. Brain Res., 696, 194 204.
30. Fix, A.S., Ross, J.F., Stitzel, S.R. Switzer, R.C. (1996) Integrated evaluation of central nervous system lesions: stains for neurons, astrocytes, and microglia reveal the spatial and temporal features of MK-801-induced neuronal necrosis in the rat cerebral cortex. Toxicol. Pathol., 24, 291 304.
31. Fix, A.S., Stitzel, S.R., Ridder, G.M. Switzer, R.C. (2000) MK-801 neurotoxicity in cupric silver-stained sections: lesion reconstruction by 3-dimensional computer image analysis. Toxicol. Pathol., 28, 84 90.
32. Friedman, H.R. Goldman-Rakic, P.S. (1988) Activation of the hippocampus and dentate gyrus by working-memory: a 2-deoxyglucose study of behaving rhesus monkeys. J. Neurosci., 8, 4693 4706.
33. Gao, X.M., Sakai, K., Roberts, R.C., Conley, R.R., Dean, B. Tamminga, C.A. (2000) Ionotropic glutamate receptors and expression of N-methyl-D-aspartate receptor subunits in subregions of human hippocampus: effects of schizophrenia. Am. J. Psychiatry, 157, 1141 1149.
34. Geyer, M. Moghaddam, B. (2002) Animal models relevant to schizophrenia disorder. In Davis, K.L., Charney, C., Coyle, J.T. Nemeroff, C. (Eds), Neuropsychopharmacology: the Fifth Generation of Progress. Lippincott Williams & Wilkins, Philadelphia, pp. 689 703.
35. Gloveli, T., Schmitz, D., Empson, R.M., Dugladze, T. Heinemann, U. (1997) Morphological and electrophysiological characterization of layer III cells of the medial entorhinal cortex of the rat. Neuroscience, 77, 629 648.
36. Gloveli, T., Behr, J., Dugladze, T., Kokaia, Z., Kokaia, M. Heinemann, U. (2003) Kindling alters entorhinal cortex-hippocampal interaction by increased efficacy of presynaptic GABA(B) autoreceptors in layer III of the entorhinal cortex. Neurobiol. Dis., 13, 203 212.
37. Hoffman, D.C. (1992) Typical and atypical neuroleptics antagonize MK-801-induced locomotion and stereotypy in rats. J. Neural Transm. Gen. Sect., 89, 1 10.
38. Hollmann, M. Heinemann, S. (1994) Cloned glutamate receptors. Annu. Rev. Neurosci., 17, 31 108.
39. Honack, D. Loscher, W. (1993) Sex differences in NMDA receptor mediated responses in rats. Brain Res., 620, 167 170.
40. Huh, K.H. Wenthold, R.J. (1999) Turnover analysis of glutamate receptors identifies a rapidly degraded pool of the N-methyl-D-aspartate receptor subunit, NR1, in cultured cerebellar granule cells. J. Biol. Chem., 274, 151 157.
41. Huppertz, B., Frank, H.G. Kaufmann, P. (1999) The apoptosis cascade - morphological and immunohistochemical methods for its visualization. Anat. Embryol. (Berl.), 200, 1 18.
42. Javitt, D.C. Zukin, S.R. (1991) Recent advances in the phencyclidine model of schizophrenia. Am. J. Psychiatry, 148, 1301 1308.
43. Lacaille, J.C. Schwartzkroin, P.A. (1988) Stratum lacunosum-moleculare interneurons of hippocampal CA1 region. II. Intrasomatic and intradendritic recordings of local circuit synaptic interactions. J. Neurosci., 8, 1411 1424.
44. Levy, W.B., Desmond, N.L. Zhang, D.X. (1998) Perforant path activation modulates the induction of long-term potentiation of the schaffer collateral-hippocampal CA1 response: theoretical and experimental analyses. Learn. Mem., 4, 510 518.
45. Lopes da Silva, F.H., Witter, M.P., Boeijinga, P.H. Lohman, A.H.M. (1990) Anatomic organization and physiology of the limbic cortex. Physiol. Rev., 70, 453 511.
46. Luby, E.D., Cohen, B.D., Rosenbaum, G., Gottlieb, J.S. Kelly, R. (1959) Study of a new schizophrenic-like drug: Sernyl. Arch. Neurol. Psychiatry, 81, 363 369.
47. Manahan-Vaughan, D., von Haebler, D., Winter, C., Juckel, G. Heinemann, U. (2007) A single application of MK-801 causes symptoms of acute psychosis, deficits in spatial memory and impairment of synaptic plasticity in rats. Hippocampus, in press. [epub ahead of print. Oct. 2007].
48. Mitsuno, K., Sasa, M., Ishihara, K., Ishikawa, M. Kikuchi, H. (1994) LTP of mossy fiber-stimulated potentials in CA3 during learning in rats. Physiol. Behav., 55, 633 638.
49. Mulkey, R.M. Malenka, R.C. (1992) Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron, 9, 967 975.
50. Olney, J.W., Labruyere, J. Price, M.T. (1989) Pathological changes induced in cerebrocortical neurons by phencyclidine and related drugs. Science, 244, 1360 1362.
51. Olney, J.W., Newcomer, J.W. Farber, N.B. (1999) NMDA receptor hypofunction model of schizophrenia. J. Psychiatr. Res., 33, 523 533.
52. Olypher, A.V., Klement, D. Fenton, A.A. (2006) Cognitive disorganization in hippocampus: a physiological model of the disorganization in psychosis. J. Neurosci., 26, 158 168.
53. Ouardouz, M. Lacaille, J.C. (1995) Mechanisms of selective long-term potentiation of excitatory synapses in stratum oriens/alveus interneurons of rat hippocampal slices. J. Neurophysiol., 73, 810 819.
54. Perez, Y., Morin, F. Lacaille, J.C. (2001) A hebbian form of long-term potentiation dependent on mGluR1a in hippocampal inhibitory interneurons. Proc. Natl Acad. Sci. USA, 98, 9401 9406.
55. Ramon y Cajal, S.R. (1893) Estructura del asta de ammon y fascial dentata. Anal. Soc. Esp. Hist. Nat., 22
56. Remondes, M. Schuman, E.M. (2002) Direct cortical input modulates plasticity and spiking in CA1 pyramidal neurons. Nature, 416, 736 740.
57. Remondes, M. Schuman, E.M. (2003) Molecular mechanisms contributing to long-lasting synaptic plasticity at the temporoammonic-CA1 synapse. Learn. Mem., 10, 247 252.
58. Remondes, M. Schuman, E.M. (2004) Role for a cortical input to hippocampal area CA1 in the consolidation of a long-term memory. Nature, 431, 699 703.
59. Rujescu, D., Bender, A., Keck, M., Hartmann, A.M., Ohl, F., Raeder, H., Giegling, I., Genius, J., McCarley, R.W., Moller, H.J. Grunze, H. (2006) A pharmacological model for psychosis based on N-methyl-D-aspartate receptor hypofunction: molecular, cellular, functional and behavioral abnormalities. Biol. Psychiatry, 59, 721 729.
60. Savaskan, N.E., Eyupoglu, I.Y., Brauer, A.U., Plaschke, M., Ninnemann, O., Nitsch, R. Skutella, T. (2000) Entorhinal cortex lesion studied with the novel dye fluoro-jade. Brain Res., 864, 44 51.
61. Schmued, L.C. Hopkins, K.J. (2000) Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res., 874, 123 130.
62. Scoville, W.B. Milner, B. (1957) Loss of recent memory after bilateral hippocampal lesions. Neurol. Neurosurg. Psychiatry, 20, 11 21.
63. Siekmeier, P.J., Hasselmo, M.E., Howard, M.W. Coyle, J. (2007) Modeling of context-dependent retrieval in hippocampal region CA1: implications for cognitive function in schizophrenia. Schizophr. Res., 89, 177 190.
64. Squire, L.R. Zola, S.M. (1997) Amnesia, memory and brain systems. Phil. Trans R. Soc. Lond. B Biol. Sci., 352, 1663 1673.
65. Steward, O. Scoville, S.A. (1976) Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J. Comp. Neurol., 169, 347 370.
66. Sturgeon, R.D., Fessler, R.G. Meltzer, H.Y. (1979) Behavioral rating scales for assessing phencyclidine-induced locomotor activity, stereotyped behavior and ataxia in rats. Eur J. Pharmacol., 59, 169 179.
67. Sybirska, E., Davachi, L. Goldman-Rakic, P.S. (2000) Prominence of direct entorhinal-CA1 pathway activation in sensorimotor and cognitive tasks revealed by 2-DG functional mapping in nonhuman primate. J. Neurosci., 20, 5827 5834.
68. Tanious, F.A., Veal, J.M., Buczak, H., Ratmeyer, L.S. Wilson, W.D. (1992) DAPI (4′,6-diamidino-2-phenylindole) binds differently to DNA and RNA: minor-groove binding at AT sites and intercalation at AU sites. Biochemistry, 31, 3103 3112.
69. Turrigiano, G.G. Nelson, S.B. (2004) Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci., 5, 97 107.
70. van Welie, I., van Hooft, J.A. Wadman, W.J. (2004) Homeostatic scaling of neuronal excitability by synaptic modulation of somatic hyperpolarization- activated Ih channels. Proc. Natl Acad. Sci. USA, 101, 5123 5128.
71. Witter, M.P., Groenewegen, H.J., Lopes da Silva, F.H. Lohman, A.H. (1989) Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog. Neurobiol., 33, 161 253.
72. Witter, M.P., Naber, P.A., Van Haeften, T., Machielsen, W.C., Rombouts, S.A., Barkhof, F., Scheltens, P. Lopes da Silva, F.H. (2000) Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways. Hippocampus, 10, 398 410.
73. Wohrl, R., von Haebler, D. Heinemann, U. (2007) Low-frequency stimulation of the direct cortical input to area CA1 induces homosynaptic LTD and heterosynaptic LTP in the rat hippocampal-entorhinal cortex slice preparation. Eur. J. Neurosci., 25, 251 258.
74. Wong, E.H., Kemp, J.A., Priestley, T., Knight, A.R., Woodruff, G.N. Iversen, L.L. (1986) The anticonvulsant MK-801 is a potent N-methyl-D-aspartate antagonist. Proc. Natl Acad. Sci. USA, 83, 7104 7108.
75. Wozniak, D.F., Dikranian, K., Ishimaru, M.J., Nardi, A., Corso, T.D., Tenkova, T., Olney, J.W. Fix, A.S. (1998) Disseminated corticolimbic neuronal degeneration induced in rat brain by MK-801: potential relevance to Alzheimer's disease. Neurobiol. Dis., 5, 305 322.