Learning impairments following injection of a selective cholinergic immunotoxin, ME20.4 IgG-saporin, into the basal nucleus of Meynert in monkeys

Neuroscience

Volumn 81, Issue 2, 1997, Pages 331-343

  Fine, A ^b   Hoyle, C ^a   Maclean, C J ^a   LeVatte, T L ^b   Baker, H F ^a   Ridley, R M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Acetylcholine; Basal nucleus; Learning; Monkey; Saporin

Indexed keywords

IMMUNOTOXIN; SAPORIN;

AGING; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; GIANT CELL; IMMUNOHISTOCHEMISTRY; LEARNING DISORDER; MONKEY; NEUROTRANSMISSION; NONHUMAN; OLIVARY NUCLEUS; PRIORITY JOURNAL;

ANIMALS; ANTIBODIES, MONOCLONAL; CALLITHRIX; FEMALE; IMMUNOTOXINS; LEARNING; MALE; N-GLYCOSYL HYDROLASES; PLANT PROTEINS; SUBSTANTIA INNOMINATA;

EID: 0031559952     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(97)00208-X     Document Type: Article

References (45)

1. Aigner T. G., Mitchell S. J., Aggleton J. P., DeLong M. R., Struble R. G., Price D. L., Wenk G. L., Mishkin M. Effects of scopolamine and physostigmine on recognition memory in monkeys with ibotenic-acid lesions of the nucleus basalis of Meynert. Psychopharmacology. 92:1987;292-300.
2. Aigner T. G., Mitchell S. J., Aggleton J. P., DeLong M. R., Struble R. G., Price D. L., Wenk G. L., Pettigrew K. D., Mishkin M. Transient impairment of recognition memory following ibotenic-acid lesions of the basal forebrain in macaques. Expl Brain Res. 86:1991;18-26.
3. Baker H. F. and Ridley R. M. (1986) Use of the common marmoset (Callithrix jacchus) in psychopharmacological research. In Working Methods in Neuropsychopharmacological Research (eds Joseph M. H. and Waddington L. J.), pp. 41-73. Manchester University Press, Manchester.
4. Baxter M. G., Bucci D. J., Gorman L. K., Wiley R. G., Gallagher M. Selective immunotoxic lesions of basal forebrain cholinergic cells: effects on learning and memory in rats. Behav. Neurosci. 109:1995;714-722.
5. Bradbury E. J., Kershaw T. R., Marchbanks R. M., Sinden J. D. Astrocyte transplants alleviate lesion induced memory deficits independently of cholinergic recovery. Neuroscience. 65:1995;955-972.
6. Dawbarn D., Allen S. J., Semenenko F. M. Co-existence of choline acetyltransferase and nerve growth factor receptors in the rat basal forebrain. Neurosci. Lett. 94:1988;138-164.
7. DiStefano P. S., Schweitzer J. B., Taniuchi M., Johnson E. M. J. Selective destruction of nerve growth factor receptor-bearing cells in vitro using a hybrid toxin composed of ricin A chain and a monoclonal antibody against nerve growth factor receptor. J. Cell Biol. 101:1985;1107-1114.
8. Dunnett S. B., Everitt B. J., Robbins T. W. The basal forebrain-cortical cholinergic system: interpreting the functional consequences of excitotoxic lesions. Trends Neurosci. 14:1991;494-501.
9. Everitt B. J., Sirkia T. E., Roberts A. C., Jones G. H., Robbins T. W. Distribution and some projections of cholinergic neurones in the brain of the common marmoset. J. comp. Neurol. 271:1988;533-558.
10. Fine A., Dunnett S. B., Björklund A., Iversen S. D. Cholinergic ventral forebrain grafts into the neocortex improved passive avoidance memory in a rat model of Alzheimer's disease. Proc. natn. Acad. Sci. U.S.A. 82:1985;5227-5230.
11. Irle E., Markowitsch H. J. Basal forebrain-lesioned monkeys are severely impaired in tasks of association and recognition memory. Ann. Neurol. 22:1987;735-743.
12. Koelle G. B. The histochemical identification of acetylcholinesterase in cholinergic, adrenergic and sensory neurons. J. Pharmac. exp. Ther. 114:1955;167-184.
13. Kordower J. H., Bartus R. T., Bothwell M., Schatteman G., Gash D. Nerve growth factor receptor immunoreactivity in the non-human primate (Cebus apella): distribution, morphology and colocalization with cholinergic enzyme. J. comp. Neurol. 277:1988;465-486.
14. Kudo Y., Shiosaka S., Matsuda M., Tohyama M. An attempt to cause the selective loss of the cholinergic neurons in the basal forebrain of the rat: a new animal model of Alzheimer's disease. Neurosci. Lett. 102:1989;125-130.
15. Leanza G., Nilsson O. G., Wiley R. G., Björklund A. Selective lesioning of the basal forebrain cholinergic system by intraventricular 192 IgG-saporin: Behavioural, biochemical and stereological studies in the rat. Eur. J. Neurosci. 7:1995;329-343.
16. Maclean C. J., Baker H. F., Fine A., Ridley R. M. The distribution of p75 neurotrophin receptor-immunoreactive cells in the forebrain of the common marmoset (Callithrix jacchus). Brain Res. Bull. 43:1996;197-208.
17. Mesulam M., Mufson E. J., Levey A. I., Wainer B. H. Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata) and hypothalamus in the rhesus monkey. J. comp. Neurol. 214:1983;170-197.
18. Mesulam M., Mufson E. J., Levey A. I., Wainer B. H. Atlas of cholinergic neurons in the forebrain and upper brainstem of the macaque based on monoclonal choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry. Neuroscience. 3:1984;669-686.
19. Mesulam M., Van Hoesen G. W. Acetylcholinesterase-rich projections from the basal forebrain of the rhesus monkey to neocortex. Brain Res. 109:1976;152-157.
20. Meunier M., Bachevalier J., Mishkin M., Murray E. A. Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys. J. Neurosci. 13:1993;5418-5432.
21. Mufson E. J., Bothwell M., Hersh L. B., Kordower J. Nerve growth factor receptor profiles in the normal, aged human basal forebrain: colocalization with cholinergic neurons. J. comp. Neurol. 285:1989;196-217.
22. Nilsson O. G., Leanza G., Rosenblad C., Lappi D. A., Wiley R. G., Björklund A. Spatial learning impairments in rats with selective immunolesion of the forebrain cholinergic system. NeuroReport. 3:1992;1005-1008.
23. Pastan I., Willingham M. C., FitzGerald D. J. P. Immunotoxins. Cell. 47:1986;641-648.
24. Ridley R. M., Aitken D. M., Baker H. F. Learning about rules but not about reward is impaired following lesions of the cholinergic projection to the hippocampus. Brain Res. 502:1989;306-318.
25. Ridley R. M., Baker H. F., Drewett B., Johnson J. A. Effects of ibotenic acid lesions of the basal forebrain on serial reversal learning in marmosets. Psychopharmacology. 86:1985;438-443.
26. Ridley R. M., Baker J. A., Baker H. F., Maclean C. J. Restoration of cognitive abilities by cholinergic grafts in cortex of monkeys with lesions of the basal nucleus of Meynert. Neuroscience. 63:1994;653-666.
27. Ridley R. M., Bowes P. M., Baker H. F., Crow T. J. An involvement of acetylcholine in object discrimination learning and memory in the marmoset. Neuropsychologia. 22:1984;253-263.
28. Ridley R. M., Gribble S., Clark B., Baker H. F., Fine A. Restoration of learning ability in fornix-transected monkeys after fetal basal forebrain but not fetal hippocampal tissue transplantation. Neuroscience. 48:1992;779-792.
29. Ridley R. M., Murray T. K., Johnson J. A., Baker H. F. Learning impairment following lesion of the basal nucleus of Meynert in the marmoset: modification by cholinergic drugs. Brain Res. 376:1986;108-116.
30. Ridley R. M., Samson N. A., Baker H. F., Johnson J. A. Visuospatial learning impairment following lesion of the cholinergic projection to the hippocampus. Brain Res. 456:1988;71-87.
31. Ridley R. M., Thornley H. D., Baker H. F., Fine A. Cholinergic neural transplants into hippocampus restore learning ability in monkeys with fornix transections. Expl Brain Res. 83:1991;533-538.
32. Ridley R. M., Timothy C. J., Maclean C. J., Baker H. F. Conditional learning and memory impairments following neurotoxic lesion of the CA1 field of the hippocampus. Neuroscience. 67:1995;263-275.
33. Ross A. H., Grob P., Bothwell M., Elder D. E., Ernst C. S., Marano N., Ghrist B. F. D., Slemp C. C., Herlyn M., Atkinson B., Koprowski H. Characterisation of nerve growth factors in neural crest tumors using monoclonal antibodies. Proc. natn. Acad. Sci. U.S.A. 81:1984;6681-6685.
34. Steckler T., Keith A. B., Wiley R. G., Sahgal A. Cholinergic lesions by 192 IgG-saporin and short-term recognition memory: role of the septohippocampal projection. Neuroscience. 66:1995;101-114.
35. Stephan H., Baron G. and Schwerdtfeger W. K. (1980) The Brain of the Common Marmoset (Callithrix jacchus); A Stereotaxic Atlas. Springer-Verlag, Berlin.
36. Torres E. M., Perry T. A., Blokland A., Wilkinson L. S., Wiley R. G., Lappi D. A., Dunnett S. B. Behavioural, histochemical and biochemical consequences of selective immunolesions in discrete regions of the basal forebrain cholinergic system. Neuroscience. 63:1994;59-122.
37. Voytko M. L. Cognitive functions of the basal forebrain cholinergic system in monkeys: memory or attention? Behav. Brain Res. 75:1996;13-25.
38. Voytko M. L., Olton D. S., Richardson R. T., Gorman I. K., Tobin J. T., Price D. L. Basal forebrain lesions in monkeys disrupt attention but not learning and memory. J. Neurosci. 14:1994;167-186.
39. Waite J. J., Chen A. D., Wardlow M. L., Wiley R. G., Lappi D. A., Thal L. J. 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. 65:1995;463-476.
40. Walsh T. J., Herzog C. D., Gandhi C., Stackman R. W., Wiley R. G. Injection of IgG 192-saporin into the medial septum produces cholinergic hypofunction and dose-dependent working memory deficits. Brain Res. 726:1996;69-79.
41. Wenk G. L., Stoehr J. D., Quintana G., Mobley S., Wiley R. G. Behavioral, biochemical, histological, and electrophysiological effects of 192 IgG-saporin injections into the basal forebrain of rats. J. Neurosci. 14:1994;5986-5995.
42. Wiley R. G., Oeltmann T. N., Lappi D. A. Immunolesioning: selective destruction of neurons using immunotoxin to rat NGF receptor. Brain Res. 562:1991;149-153.
43. Winkler J., Suhr S. T., Gage F. H., Thal L. J., Fisher L. J. Essential role of neocortical acetylcholine in spatial memory. Nature. 375:1995;484-487.
44. Zola-Morgan S., Squire L. R. Memory impairments in monkeys following lesions limited to the hippocampus. Behav. Neurosci. 100:1986;155-160.
45. Zola-Morgan S., Squire L. R., Amaral D. G., Suzuki W. A. Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment. J. Neurosci. 9:1989;4355-4370.