Potentiation of glutamatergic EPSPs in rat CA1 hippocampal neurons after selective cholinergic denervation by 192 IgG-saporin

Synapse

Volumn 26, Issue 3, 1997, Pages 292-300

  Jouvenceau, Anne ^a,b   Billard, Jean Marie ^a   Lamour, Yvon ^a   Dutar, Patrick ^a  

^a Lab Physpharmacol du Syst Nerveux   (France)

^b INSERM   (France)

Author keywords

192 IgG saporin; acetylcholine; excitatory postsynaptic potential; glutamate receptors; hippocampus; inhibitory postsynaptic potential; pyramidal cells; rat

Indexed keywords

4 AMINOBUTYRIC ACID; ACETYLCHOLINE; GLUTAMATE RECEPTOR; GLUTAMIC ACID; IMMUNOGLOBULIN G; IMMUNOTOXIN; N METHYL DEXTRO ASPARTIC ACID; SAPORIN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; HISTOCHEMISTRY; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT;

ANIMALS; ANTIBODIES, MONOCLONAL; CHOLINERGIC AGENTS; ELECTROPHYSIOLOGY; EVOKED POTENTIALS; GLUTAMIC ACID; HIPPOCAMPUS; HISTOCYTOCHEMISTRY; IMMUNOTOXINS; INJECTIONS, INTRAVENTRICULAR; MALE; MEMBRANE POTENTIALS; N-GLYCOSYL HYDROLASES; NEURONS; PARASYMPATHECTOMY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 0030961529     PISSN: 08874476     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-2396(199707)26:3<292::AID-SYN10>3.0.CO;2-Y     Document Type: Article

References (54)

1. Bartus, R.T., Dean, R.L., Beer, B., and Lippa A.S. (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science, 17:408-417.
2. Baudry, M., and Massicotte, G. (1992) Physiological and pharmacological relationships between long-term potentiation and mammalian memory. Concepts Neurosci., 3:79-98.
3. Bliss, T.V.P., and Collingridge, G.L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature, 36:31-39.
4. Collingridge, G.L., Kehl, S.J., and McLennan, H. (1983) Excitatory amino acids in synaptic transmission in the schaffer commissural pathway of the rat hippocampus. J. Physiol. (Lond.), 334:33-46.
5. Crutcher, K.A., Brothers, L., and Davis, J.N. (1981) Sympathetic noradrenergic sprouting in response to central cholinergic denervation: a histochemical study of neuronal sprouting in the rat hippocampal formation. Brain Res., 210:115-128.
6. B autoreceptors in rat hippocampus. J. Physiol. (Lond.), 472:245-265.
7. Davies, C.H., Davies, S.N., and Collingridge, G.L. (1990) Paired-pulse depression of monosynaptic GABA-mediated inhibitory postsynaptic responses in rat hippocampus. J. Physiol. (Lond.), 424:513-531.
8. B autoreceptors regulate the induction of LTP. Nature, 349: 609-611.
9. Dingledine, R., Hynes, M.A., and King, G.L. (1986) Involvement of N-methyl-D-aspartate receptors in epileptiform bursting in the rat hippocampal slice. J. Physiol., 380:175-189.
10. Foster, T.C., and McNaughton, B.L. (1991) Long-term enhancement of CA1 synaptic transmission is due to increased quantal size, not quantal content. Hippocampus, 1:79-92.
11. Gasser, U.E., and Dravid, A.R. (1987) Noradrenergic, serotonergic, and cholinergic sprouting in the hippocampus that follows partial or complete transection of the septohippocampal pathway: contributions of spared inputs. Exp. Neurol., 96:352-364.
12. Geddes, J.W., Brunner, L., Cotman, C.W., and Kuzsaki, G. (1992) Alterations in [3H]kainate and N-methyl-D-aspartate-sensitive L-[3H]-glutamate binding in the rat hippocampal formation following fimbria-fornix lesions. Exp. Neurol., 115:271-281.
13. Greenamyre, J.T., and Maragos, W.F. (1993) Neurotransmitter receptors in Alzheimer's disease. Cerebrovascular Brain Metabol. Rev., 5:61-94.
14. Hagan, J.J., and Morris, R.G.M. (1988) The cholinergic hypothesis of memory: a review of animal experiments. In: Handbook of Psychopharmacology, vol. 20. pp. 237-323.
15. Harata, N., Ebihara, S., and Akaike, N. (1992) Modulation of NMDA receptors by ACh in the central nervous system. Prog. Neuropsychopharmacol. Biol. Psychiatry, 16:977-984.
16. Heckers, S., Ohtake, T., Wiley, R.G., Lappi, D.A., Geula, C., and Mesulam, M-M. (1994) Complete and selective cholinergic denervation of rat neocortex and hippocampus but not amygdala by an immunotoxin against the p75 NGF receptor. J. Neurosci., 14:1271-1289.
17. Herron, C.E., Williamson, R., and Collingridge, G.L. (1985) A selective N-methyl-D-aspartate antagonist depresses epileptiform activity in rat hippocampal slices. Neurosci. Lett., 61:255-260.
18. Hess, G., Kuhnt, V., and Voronin, L.L. (1987) Quantal analysis of paired-pulse facilitation in guinea pig hippocampal slices. Neurosci. Lett., 77:187-192.
19. Hounsgaard, J. (1978) Presynaptic inhibitory action of acetylcholine in area CA1 of the hippocampus. Exp. Neurol., 62:787-797.
20. Jackisch, R., Neufang, B., Hertting, G., Jeltsch, H., Kelche, C., Will, B., and Cassel, J.C. (1995) Sympathetic sprouting: time course of changes of noradrenergic, cholinergic, and serotonergic markers in the denervated rat hippocampus. J. Neurochem., 65:329-337.
21. Jouvenceau, A., Billard, J-M., Wiley, R.G., Lamour, Y., and Dutar, P. (1994) Cholinergic denervation of the rat hippocampus by 192 IgG-saporin: electrophysiological evidence. NeuroReport, 5:1781-1784.
22. Jouvenceau, A., Billard, J-M., Lamour, Y., and Dutar, P. (1996) Persistence of CA1 hippocampal LTP after selective cholinergic denervation. NeuroReport, 7:948-952.
23. Karnovsky, M.J., and Roots, L. (1964) A "direct-coloring" thiocholine method for cholinesterases. J. Histochem. Cytochem., 12:219-221.
24. Kauer, J.A., Malenka, R.C., and Nicoll, R.A. (1988) NMDA application potentiates synaptic transmission in the hippocampus. Nature, 334:250-252.
25. Kokaia, M., Ferencz, I., Leanza, G., Elmer, E., Metsis, M., Kokaia, Z., Wiley, R.G., and Lindvall, O. (1996) Immunolesioning of basal forebrain cholinergic neurons facilitates hippocampal kindking and perturbs neurotrophin messenger RNA regulation. Neuroscience 70:313-327.
26. Leanza, G., Nilsson, O.G., Wiley, R.G., and Björklund, A. (1995) Selective lesioning of the basal forebrain cholinergic system by intraventricular 192 IgG-saporin: behavioural, biochemical and stereological studies in the rat. Eur. J. Neurosci., 7:329-343.
27. Lindefors, N., Boatell, M.L., Mahy, N., and Person, H. (1992) Wide-spread neuronal degeneration after ibotenic acid lesioning of cholinergic neurons in the nucleus basalis revealed by in situ hybridization. Neurosci. Lett., 135:262-264.
28. Lynch, G., Stanfield, B., and Cotman, C. (1973) Developmental differences in postlesion axonal growth in the hippocampus. Brain Res., 59:155-168.
29. Marchi, M., Bocchieri, P., Garbarino, L., and Raiteri, M. (1989) Muscarinic inhibition of endogenous glutamate release from rat hippocampus synaptosomes. Neurosci. Lett., 96:229-234.
30. Markram, H., and Segal, M. (1990) Long-lasting facilitation of excitatory postsynaptic potentials in the rat hippocampus by acetylcholine. J. Physiol. (Lond.), 427:381-393.
31. Markram, H., and Segal, M. (1992) The inositol 1,4,5-trisphosphate pathway mediates cholinergic potentiation of rat hippocampal neuronal responses to NMDA. J. Physiol. (Lond.), 447:513-533.
32. Monaghan, D.T., Bridges, R.J., and Cotman, C.W. (1989) The excitatory amino acid receptors: their classes pharmacology and distinct properties in the function of the central nervous system. Annu. Rev. Pharm. Toxicol., 29:365-402.
33. B-receptor-mediated inhibition of the N-methyl-D-aspartate component of synaptic transmission in the rat hippocampus. J. Neurosci., 11:203-209.
34. B autoreceptors mediate activity-dependent disinhibition and enhance signal transmission in the dentate gyrus. J. Neurophysiol., 69:674-691.
35. Nilsson, O.G., Leanza, G., Rosenblad, C., Lappi, D.A., Wiley, R.G., and Björklund, A. (1992) Spatial learning impairments in rats with selective immunolesion of the forebrain cholinergic system. NeuroReport, 3:1005-1008.
36. B receptors of glutamatergic excitation and GABAergic inhibition of neostriatal neurons. J. Neurophysiol., 67:477-481.
37. Paxinos, G., and Watson, C. (1986) The Rat Brain in Stereotaxic Coordinates. Academic Press, New York.
38. Pepeu, G., Casamenti, F., Marconcini Pepeu, I., and Scali, C. (1993) The brain cholinergic system in ageing mammals. J. Reprod. Fertil., suppl. 46:155-162.
39. Pitler, T.A., and Alger, B.E. (1992) Cholinergic excitation of GABAergic interneurons in the rat hippocampal slice. J. Physiol. (Lond.), 450:127-142.
40. Roßner, S., Schliebs, R., and Bigl, V. (1994) Ibotenic acid lesion of nucleus basalis magnocellularis differentially affects cholinergic, glutamatergic and GABAergic markers in cortical rat brain regions. Brain Res., 668:85-99.
41. Roßner, S., Schliebs, R., and Bigl, V. (1995) 192 IgG-saporin induced immunotoxic lesions of cholinergic basal forebrain system differentially affect glutamatergic and GABAergic markers in cortical rat brain regions. Brain Res., 696:165-176.
42. Roepstorff, A., and Lambert, J.D.C. (1992) Manipulations of the synaptic concentration of GABA and paired-pulse depression of the IPSP in hippocampal CA1 pyramidal neurones. Pharmacol. Comm., 2:120.
43. Schauwecker, P.E., and McNeill, T.H. (1995) Enhanced but delayed axonal sprouting of the commissural/associational pathway following a combined entorhinal cortex/fimbria fornix lesion. J. Comp. Neurol., 351:453-464.
44. Schoepp, D.A., and Conn, P.J. (1993) Metabotropic glutamate receptors in brain function and pathology. TIPS, 14:13-19.
45. Segal, M. (1989) Presynaptic cholinergic inhibition in hippocampal cultures. Synapse, 4:305-312.
46. Steckler, T., Keith, A.B., Wiley, R.G., and Sahgal, A. (1995) Cholinergic lesions by 192 IgG-saporin and short-term recognition memory: role of the septohippocampal projection. Neuroscience, 66:101-114.
47. Torres, E.M., Blokland, A., Wilkinson, L.S., Wiley, R.G., Lappi, D.A., and Dunnett, S.B. (1994) Behavioural, histochemical and biochemical consequences of selective immunolesions in discrete regions of the basal forebrain cholinergic system. Neuroscience, 63:95-122.
48. Ulas, J., Monaghan, D.T., and Cotman, C.W. (1990a) Kainate receptors in the rat hippocampus: a distribution and time course of changes in response to unilateral lesions of the entorhinal cortex. J. Neurosci., 10:2352-2362.
49. Ulas, J., Monaghan, D.T., and Cotman, C.W. (1990b) Plastic response of hippocampal excitatory amino acid receptors to deafferentation and reinnervation. Neuroscience, 34:9-17.
50. Valentino, R.J., and Dingledine, R. (1981) Presynaptic inhibitory effect of acetylcholine in the hippocampus. J. Neurosci., 1:784-792.
51. Waite, J.J., Chen, A.D., Wardlow, M.L., Wiley, R.G., Lappi, D.A., and Thal, L.J. (1995) 192 immunoglobulin G-saporin produces graded behavioral and biochemical changes accompanying the loss of cholinergic neurons of the basal forebrain and cerebellar Purkinje cells. Neuroscience, 65:463-476.
52. Walsh, T.J., Kelly, R.M., Dougherty, K.D., Stackman, R.W., Wiley, R.G., and Kutscher, C.L. (1995) Behavioral and neurobiological alterations induced by the immunotoxin 192 IgG-saporin: cholinergic and non-cholinergic effects following i.c.v. injection. Brain Res., 702:233-245.
53. Wiley, R.G., and Lappi, D.A. (1993) Preparation of anti-neuronal immunotoxins for selective neural immunolesioning. Neurosci. Protocols, 93-020-02-01-12.
54. Wiley, R.G., Oeltmann, T.N., and Lappi, D.A. (1991) Immunolesioning: selective destruction of neurons using immunotoxin to rat NGF receptor. Brain Res., 562:149-153.