Hippocampal grafts of acetylcholine-producing cells are sufficient to improve behavioural performance following a unilateral fimbria-fornix lesion

Neuroscience

Volumn 84, Issue 3, 1998, Pages 771-781

  Dickinson Anson, H ^a   Aubert, I ^a   Gage, F H ^a   Fisher, L J ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Acetylcholine; Choline acetyltransferase; Engineered cells; Hippocampus; Learning memory; Water maze

Indexed keywords

ACETYLCHOLINE; CHOLINE ACETYLTRANSFERASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN FORNIX; BRAIN INJURY; CELL TRANSPLANTATION; CONTROLLED STUDY; HIPPOCAMPUS; LEARNING; LOCOMOTION; MALE; MAZE TEST; MEMORY; NONHUMAN; PRIORITY JOURNAL; RAT;

ACETYLCHOLINE; ACETYLCHOLINESTERASE; ANIMALS; BEHAVIOR, ANIMAL; BRAIN TISSUE TRANSPLANTATION; CELL TRANSPLANTATION; CEREBRAL CORTEX; DROSOPHILA; FIBROBLASTS; HABITUATION, PSYCHOPHYSIOLOGIC; HIPPOCAMPUS; MALE; MAZE LEARNING; MEMORY; MOTOR ACTIVITY; NEURONS; RATS; RATS, INBRED F344;

EID: 0032562162     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(97)00543-5     Document Type: Article

References (76)

1. Auerbach J. M., Segal M. A novel cholinergic induction of long-term potentiation in rat hippocampus. J. Neurophysiol. 72:1994;2034-2040.
2. Bartus R. T., Dean R. L., Beer B., Lippa A. S. The cholinergic hypothesis of geriatric memory dysfunction. Science. 217:1982;408-417.
3. Björklund A., Stenevi U. Reformation of the severed septohippocampal cholinergic pathway in the adult rat by transplanted septal neurons. Cell Tiss. Res. 185:1977;289-302.
4. Bland B. H., Colom L. V., Konopacki J., Roth S. H. Intracellular records of carbachol-induced theta rhythm in hippocampal slices. Brain Res. 447:1988;364-368.
5. Blitzer R. D., Gil O., Landau E. Cholinergic stimulation enhances long-term potentiation in the CA1 region of rat hippocampus. Neurosci. Lett. 119:1990;207-210.
6. Brito G. N. O., Brito L. S. O. Septohippocampal system and the prelimbic sector of frontal cortex: a neuropsychological battery analysis in the rat. Behav. Brain Res. 36:1990;127-146.
7. Brito G. N. O., Davis B. J., Stopp L. C., Stanton M. E. Memory and the septohippocampal cholinergic system in the rat. Psychopharmacology. 81:1983;315-320.
8. Buzsaki G., Gage F. H., Czopf J., Björklund A. Restoration of rhythmic slow activity (theta) in the subcortically denervated hippocampus by fetal CNS transplants. Brain Res. 400:1987;334-347.
9. Cassel J. C., Kelche C., Will B. Time-dependent effects of intrahippocampal grafts in rats with fimbria-fornix lesions. Expl Brain Res. 81:1990;179-190.
10. Cassel J. C., Neufang B., Kelche C., Aiple F., Will B. E., Hertting G., Jackisch R. Effects of septal and/or raphe cell suspension grafts on hippocampal choline acetyltransferase activity, high affinity synaptosomal uptake of choline and serotonin, and behavior in rats with extensive septohippocampal lesions. Brain Res. 585:1992;243-254.
11. Chandler C. E., Parson L. M., Hosang M., Shooter E. M. A monoclonal antibody modulates the interaction of nerve growth factor with PC12 cells. J. biol. Chem. 259:1984;6882-6889.
12. Clarke D. J., Gage F. H., Björklund A. Formation of cholinergic synapses by intrahippocampal septal grafts as revealed by choline acetyltransferase immunohistochemistry. Brain Res. 369:1986;151-162.
13. Cole A. E., Nicoll R. A. Acetylcholine mediates a slow synaptic potential in hippocampal pyramidal cells. Science. 221:1983;1299-1301.
14. Daniloff J. K., Bodony R. P., Low W. C., Wells J. Cross-species embryonic septal transplants: restoration of conditioned learning behavior. Brain Res. 346:1985;176-180.
15. Danks A. M., Oestreicher A. B., Spruijt B. M., Gispen W. H., Isaacson R. L. Behavioral and anatomical consequences of unilateral fornix lesions and administration of nimodipine. Brain Res. 557:1991;308-312.
16. Dawson V. L., Gage F. H., Hunt M. A., Wamsley J. K. Normalization of subtype-specific muscarinic receptor binding in the denervated hippocampus by septodiagonal band grafts. Expl Neurol. 106:1989;115-124.
17. Decker M. W. The effects of aging on hippocampal and cortical projections of the forebrain cholinergic system. Brain Res. Rev. 12:1987;423-438.
18. Decker M. W., Majchrzak M. J., Anderson D. J. Effects of nicotine on spatial memory deficits in rats with septal lesions. Brain Res. 572:1992;281-285.
19. Decker M. W., Tran T., McGaugh J. L. A comparison of the effects of scopolamine and diazepam on acquisition and retention of inhibitory avoidance in mice. Psychopharmacology. 100:1990;515-521.
20. Dunnett S. B. (1994) Strategies for testing learning and memory abilities in transplanted rats. In Functional Neural Transplantation (eds Dunnett S. B. and Björklund A.), pp. 217-251. Raven, New York.
21. Dunnett S. B. Neural transplantation in animal models of dementia. Eur. J. Neurosci. 2:1990;567-587.
22. Dunnett S. B., Low W. C., Iversen S. D., Stenevi U., Björklund A. Septal transplants restore maze learning in rats with fimbria-fornix lesions. Brain Res. 251:1982;335-348.
23. Eichenbaum H., Otto T., Cohen N. J. The hippocampus - what does it do? Behav. neural Biol. 57:1992;2-36.
24. Fischer W., Gage F. H., Björklund A. Degenerative changes in forebrain cholinergic nuclei correlate with cognitive impairments in aged rats. Eur. J. Neurosci. 1:1989;34-45.
25. Fisher L. J., Schinstine M., Salvaterra P., Dekker A. J., Thal L. J., Gage F. H. In vivo production and release of acetylcholine from primary fibroblasts genetically modified to express choline acetyltransferase. J. Neurochem. 61:1993;1323-1332.
26. Fonnum F. (1975) Radiochemical assays for choline acetyltransferase and acetylcholinesterase. In Research in Neurochemistry (eds Marks N. and Rodnight R.), pp 253-275. Plenum, New York.
27. Freund T. F., Antal M. GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature. 336:1988;170-173.
28. Gage F. H. and Björklund A. (1986) Compensatory collateral sprouting of aminergic systems in the hippocampal formation following partial deafferentation. In The Hippocampus (eds Isaccson R. L. and Pribram K. H.), pp. 33-63. Plenum Press, New York.
29. Gage F. H., Chen K. S., Buzsaki G., Armstrong D. Experimental approaches to age-related cognitive impairments. Neurobiol. Aging. 9:1988;645-655.
30. Gage F. H., Björklund A., Stenevi U. Reinnervation of the partially deafferented hippocampus by compensatory collateral sprouting from spared cholinergic and noradrenergic afferents. Brain Res. 268:1983;27-37.
31. Gage F. H., Wictorin K., Fischer W., Williams L. R., Varon S., Björklund A. Retrograde cell changes in medial septum and diagonal band following fimbria-fornix transection: quantitative temporal analysis. Neuroscience. 19:1986;241-255.
32. Ghoneim M. M., Mewaldt S. P. Effects of diazepam and scopolamine on storage, retrieval and organizational processes in memory. Psychopharmacologia. 44:1975;257-262.
33. Gibbs R. B. K., Anderson K., Cotman C. W. Factors affecting innervation of the CNS: comparison of three cholinergic cell types transplanted to the hippocampus of adult rats. Brain Res. 383:1986;362-366.
34. Hedreen J. C., Bacon J. C., Price D. L. A modified histochemical method to visualize acetylcholinesterase-containing axons. J. Histochem. Cytochem. 33:1985;134-140.
35. Hefti F. Nerve growth factor promotes survival of septal cholinergic neurons after fimbrial transections. J. Neurosci. 6:1986;2155-2162.
36. Hodges H., Allen Y., Sinden J., Lantos P. L., Gray J. A. Effects of cholinergic-rich neural grafts on radial maze performance of rats after excitotoxic lesions of the forebrain cholinergic projection system. II. Cholinergic drugs as probes to investigate lesion-induced deficits and transplant-induced functional recovery. Neuroscience. 45:1991;609-623.
37. Howard M. A., Gross A., Grady M. S., Langer R. S., Mathiowitz E., Winn H. R., Mayberg M. R. Intracerebral drug delivery in rats with lesion-induced memory deficits. J. Neurosurg. 71:1989;105-112.
38. Huerta P. T., Lisman J. E. Heightened synaptic plasticity of hippocampal CA1 neurons during a cholinergically induced rhythmic state. Nature. 364:1993;723-725.
39. Jeltsch H., Cassel J. C., Neufang B., Kelche C., Heritting G., Jackisch R., Will B. The effects of intrahippocampal raphe and/or septal grafts in rats with fimbria-fornix lesions depend on the origin of the grafted tissue and the behavioural task used. Neuroscience. 63:1994;19-39.
40. Joyce J. N., Gibbs R. B., Cotman C. W., Marshall J. F. Regulation of muscarinic receptors in hippocampus following cholinergic denervation and reinnervation by septal striatal transplants. J. Neurosci. 9:1989;2776-2791.
41. Kawaja M. D., Gage F. H. Morphological and neurochemical features of cultured primary skin fibroblasts of Fischer 344 rats following striatal implantation. J. comp. Neurol. 317:1992;102-116.
42. Kitajima I., Yamamoto T., Ohno M., Ueki S. Working and reference memory in rats in the three-panel runway task following dorsal hippocampal lesions. Jap. J. Pharmac. 58:1992;175-183.
43. Konopacki J., MacIver M. B., Bland B. H., Roth S. H. Carbachol-induced EEG "theta" activity in hippocampal brain slices. Brain Res. 405:1987;196-198.
44. Kraemer P. J., Brown R. W., Baldwin S. A., Scheff S. W. Validation of a single-day Morris water maze procedure used to assess cognitive deficits associated with brain damage. Brain Res. Bull. 39:1996;17-22.
45. Kromer L. F. Cholinergic axons from delayed septal implants and sympathetic fibers co-exist in the denervated dentate gyrus. Brain Res. Bull. 9:1982;539-544.
46. Lapchak P. A., Araujo D. M., Hefti F. Regulation of hippocampal muscarinic receptor function by chronic nerve growth factor treatment in adult rats with fimbrial transections. Neuroscience. 53:1993;379-394.
47. Levey A. L., Edmunds S. M., Koliatsos V., Wiley R. G., Heilman C. J. Expression of m1-m4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulation by cholinergic innervation. J. Neurosci. 15:1995;4077-4092.
48. Li Y. J., Simon J. R., Low W. C. Intrahippocampal grafts of cholinergic-rich striatal tissue ameliorate spatial memory deficits in rats with fornix lesions. Brain Res. Bull. 29:1992;147-155.
49. Lippa A. S., Pelham R. W., Beer B., Critchett D. J., Dean R. L., Bartus R. T. Brain cholinergic dysfunction and memory in aged rats. Neurobiol. Aging. 1:1980;13-19.
50. Low W. C., Lewis P. R., Bunch S. T., Dunnett S. B., Thomas S. R., Iversen S. D., Björklund A., Stenevi U. Functional recovery following neural transplantation of embryonic septal nuclei in adult rats with septohippocampal lesions. Nature. 300:1982;260-262.
51. Madison D. V., Lancaster B., Nicoll R. A. Voltage clamp analysis of cholinergic action in the hippocampus. J. Neurosci. 7:1987;733-741.
52. Maho C., Dutrieux G., Ammassari-Teule M. Parallel modifications of spatial memory performances, exploration patterns, and hippocampal theta rhythms in fornix-damaged rats: reversal by oxotremorine. Behav. Neurosci. 102:1988;601-604.
53. Matsuoka N., Maeda N., Ohkubo Y., Yamaguchi I. Differential effects of physostigmine and pilocarpine on the spatial memory deficits produced by two septohippocampal deafferentations in rats. Brain Res. 559:1991;233-240.
54. 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.
55. Morris R. G. M. (1983) An attempt to dissociate "spatial mapping" and "working memory" theories of hippocampal function. In The Neurobiology of the Hippocampus (ed. Seifert W.) pp. 405-432. Academic, London.
56. Morrow A. L., Loy R., Creese I. Alteration of nicotinic cholinergic binding sites in hippocampus after fimbria transection. Brain Res. 334:1985;309-314.
57. Niijima J., Chalmers G. R., Peterson D. A., Fisher L. J., Patterson P. H., Gage F. H. Enhanced survival and neuronal differentiation of adrenal chromaffin cells cografted into the striatum with NGF-producing fibroblasts. J. Neurosci. 15:1995;1180-1194.
58. Nilsson O. G., Gage F. H. Anticholinergic sensitivity in the aging rat septohippocampal system as assessed in a spatial memory task. Neurobiol. Aging. 14:1993;487-497.
59. Nilsson O. G., Brundin P., Björklund A. Amelioration of spatial memory impairment by intrahippocampal grafts of mixed septal and raphe tissue in rats with combined cholinergic and serotonergic denervation of the forebrain. Brain Res. 515:1990;193-200.
60. Nilsson O. G., Shapiro M. L., Gage F. H., Olton D. S., Björklund A. Spatial learning and memory following fimbria-fornix transection and grafting of fetal septal neurons to the hippocampus. Expl Brain Res. 67:1987;195-215.
61. Ohno M., Yamamoto T., Watanabe S. Blockade of hippocampal nicotinic receptors impairs working memory but not reference memory in rats. Pharmac. Biochem. Behav. 45:1993;89-93.
62. Olton D. S., Givens B., Markowska A. L., Shapiro M. and Golski S. (1991) Mnemonic functions of the cholinergic septohippocampal system. In Memory: Organization and Locus of Change (eds Squire L. R., Weinberger N. M. and McGaugh J. L.), pp. 250-269. Oxford University Press, Oxford.
63. Olton D. S., Walker J. A., Wolf W. A. A disconnection analysis of hippocampal formation. Brain Res. 233:1982;241-253.
64. Paxinos G. and Watson C. (1986) The Rat Brain in Stereotaxic Coordinates. Academic, CA.
65. Richter-Levin G., Greenberger V., Segal M. Regional specificity of raphe graft-induced recovery of behavioral functions impaired by combined serotonergic/cholinergic lesions. Expl Neurol. 121:1993;256-260.
66. 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.
67. Sara S. J., Dyon-Laurent C., Guibert B., Leviel V. Noradrenergic hyperactivity after partial fornix section: role in cholinergic dependent memory performance. Expl Brain Res. 89:1992;125-132.
68. Schinstine M., Rosenberg M. B., Routledge-Ward C., Friedmann T., Gage F. H. Effects of choline and quiescence on Drosophila choline acetyltransferase expression and acetylcholine production by transduced rat fibroblasts. J. Neurochem. 58:1992;2019-2029.
69. Segal M. Presynaptic cholinergic inhibition in hippocampal cultures. Synapse. 4:1989;305-312.
70. Shapiro M. L., Simon D. K., Olton D. S., Gage F. H., Nilsson O., Björklund A. Intrahippocampal grafts of fetal basal forebrain tissue alter place fields in the hippocampus of rats with fimbria-fornix lesions. Neuroscience. 32:1989;1-18.
71. Spruijt B., Pitsikas N., Algeri S., Gispen W. H. Org2766 improves performance of rats with unilateral lesions in the fimbria fornix in a spatial learning task. Brain Res. 527:1990;192-197.
72. Tarricone B. J., Keim S. R., Simon J. R., Low W. C. Intrahippocampal transplants of septal cholinergic neurons: high affinity choline uptake and spatial memory function. Brain Res. 548:1991;55-62.
73. Tucek S. (1978) Acetylcholine Synthesis in Neurons. Chapman and Hall, London.
74. Whishaw I. Q. Cholinergic receptor blockade in the rat impairs locale but not taxon strategies for place navigation in a swimming pool. Behav. Neurosci. 99:1985;979-1005.
75. Whishaw I. Q., Jarrard L. E. Similarities vs differences in place learning and circadian activity in rats after fimbria-fornix section or ibotenate removal of hippocampal cells. Hippocampus. 5:1995;595-604.
76. Winkler J., Suhr S., Gage F. H., Thal L. J., Fisher L. J. Essential role of neocortical acetylcholine in spatial memory. Nature. 375:1995;484-487.