Time course of behavioral changes following basal forebrain cholinergic damage in rats: Environmental enrichment as a therapeutic intervention

Neuroscience

Volumn 132, Issue 1, 2005, Pages 13-32

  Paban, V ^a   Jaffard, M ^a   Chambon, C ^a   Malafosse, M ^a   Alescio Lautier, B ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

Author keywords

192 IgG saporin; Memory; Nonmatching to position; Object location; Object recognition

Indexed keywords

IMMUNOGLOBULIN G; IMMUNOTOXIN; SAPORIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN INJURY; CHOLINERGIC ACTIVITY; CHOLINERGIC SYSTEM; COGNITION; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; FOREBRAIN; IMMUNOHISTOCHEMISTRY; MALE; MAZE TEST; MEMORY DISORDER; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; RECOGNITION; TASK PERFORMANCE;

EID: 15044365376     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2004.11.024     Document Type: Article

References (78)

1. M. Ammassari-Teule, A. Tozzi, C. Rossi-Arnaud, E. Save, C. Thinus-Blanc Reactions to spatial and nonspatial change in two inbred strains of mice further evidence supporting the hippocampal dysfunction hypothesis in the DBA/2 strain Psychobiology 23 1995 284 289
2. A.M. Bailey, M.L. Rudisill, E.J. Hoof, M.L. Loving 192 IgG-saporin lesions to the nucleus basalis magnocellularis (nBM) disrupt acquisition of learning set formation Brain Res 969 2003 147 159
3. R.T. Bartus, R.L. Dean, B. Beer, A.S. Lippa The cholinergic hypothesis of geriatric memory dysfunction Science 217 1982 408 417
4. M.G. Baxter Effects of selective immunotoxic lesions on learning and memory Methods Mol Biol 166 2001 249 265
5. M.G. Baxter, D.J. Bucci, L.K. Gorman, R.G. Wiley, M. Gallagher Selective immunotoxic lesions of basal forebrain cholinergic cells effects on learning and memory in rats Behav Neurosci 109 1995 714 722
6. N.C. Berchtold, J.P. Kesslak, C.W. Cotman Hippocampal brain-derived neurotrophic factor gene regulation by exercise and the medial septum J Neurosci Res 68 2002 511 521
7. J. Berger-Sweeney, S. Heckers, M.M. Mesulam, R.G. Wiley, D.A. Lappi, M. Sharma Differential effects on spatial navigation of immunotoxin-induced cholinergic lesions of the medial septal area and nucleus basalis magnocellularis J Neurosci 14 1994 4507 4519
8. J.L. Bizon, J.S. Han, C. Hudon, M. Gallagher Effects of hippocampal cholinergic deafferentation on learning strategy selection in a visible platform version of the water maze Hippocampus 13 2003 676 684
9. S.E. Browne, L. Lin, A. Mattsson, B. Georgievska, O. Isacson Selective antibody-induced cholinergic cell and synapse loss produce sustained hippocampal and cortical hypometabolism with correlated cognitive deficits Exp Neurol 170 2001 36 47
10. Y. Chudasama, J.W. Dalley, F. Nathwani, P. Bouger, T.W. Robbins Cholinergic modulation of visual attention and working memory dissociable effects of basal forebrain 192-IgG-saporin lesions and intraprefrontal infusions of scopolamine Learn Mem 11 2004 78 86
11. R.E. Clark, S.M. Zola, L.R. Squire Impaired recognition memory in rats after damage to the hippocampus J Neurosci 20 2000 8853 8860
12. D. Collerton Cholinergic function and intellectual decline in Alzheimer's disease Neuroscience 19 1986 1 28
13. C.W. Cotman, N.C. Berchtold Exercise a behavioral intervention to enhance brain health and plasticity Trends Neurosci 25 2002 295 301
14. A.C. Cuello, L. Garofalo, D. Maysinger, E.P. Pioro, A.R. Da Silva Injury and repair of central cholinergic neurons Prog Brain Res 84 1990 301 311
15. A.J.A.M. Dekker, D.J. Connor, L.J. Thal The role of cholinergic projections from the nucleus basalis in memory Neurosci Biobehav Rev 15 1990 299 317
16. A. Ennaceur, J. Delacour A new one-trial test for neurobiological studies of memory in rats Behav Brain Res 31 1988 4 59
17. R.M. Escorihuela, A. Fernandez-Tereul, A. Tobena, N.M. Vivas Early environmental stimulation produces long-lasting changes on beta-adrenoceptor transduction Neurobiol Learn Mem 64 1995 49 57
18. B.J. Everitt, T.W. Robbins Central cholinergic systems and cognition Annu Rev Psychol 48 1997 649 684
19. A.J. Fulford, S. Butler, D.J. Heal, D.A. Kendall, C.A. Marsden Evidence for altered a2-adrenoreceptor function following isolation rearing in the rat Psychopharmacology 116 1994 183 190
20. R. Galani, O. Lehmann, T. Bolmont, E. Aloy, F. Bertrand, C. Lazarus, H. Jeltsch, J.C. Cassel Selective immunolesions of CH4 cholinergic neurons do not disrupt spatial memory in rats Physiol Behav 76 2002 75 90
21. R.P. Gaykema, C. Nyakas, E. Horvath, L.B. Hersh, C. Majtenyi, P.G. Luiten Cholinergic fiber aberrations in nucleus basalis lesioned rat and Alzheimer's disease Neurobiol Aging 13 1992 441 448
22. R.J. Hamm, M.D. Temple, D.M. O'Dell, R.B. Pike, B.G. Lyeth Exposure to environmental complexity promotes recovery of cognitive function after traumatic brain injury J Neurotrauma 13 1996 41 47
23. S. Heckers, T. Ohtake, R.G. Wiley, D.A. Lappi, C. Geula, M.M. Mesulam Complete and selective cholinergic denervation of rat neocortex and hippocampus but not amygdala by an immunotoxin against the p75 NGF receptor J Neurosci 14 1994 1271 1289
24. B.R. Ickes, T.M. Pham, L.A. Sanders, D.S. Albeck, A.H. Mohammed, A.C. Granholm Long-term environmental enrichment leads to regional increases in neurotrophin levels in rat brain Exp Neurol 164 2000 45 52
25. L.S. Janis, M.M. Glasier, Z. Fulop, D.G. Stein Intraseptal injections of 192 IgG saporin produce deficits for strategy selection in spatial-memory tasks Behav Brain Res 90 1998 23 34
26. D.A. Johnson, N.J. Zambon, R.B. Gibbs Selective lesion of cholinergic neurons in the medial septum by 192 IgG-saporin impairs learning in a delayed matching to position T-maze paradigm Brain Res 943 2002 132 141
27. G. Kempermann, H.G. Kuhn, F.H. Gage Experience-induced neurogenesis in the senescent dentate gyrus Neuroscience 18 1998 3206 3212
28. B.P. Kirby, J.N. Rawlins The role of the septo-hippocampal cholinergic projection in T-maze rewarded alternation Behav Brain Res 143 2003 41 48
29. S. Kobayashi, Y. Ohashi, S. Ando Effects of enriched environments with different durations and starting times on learning capacity during aging in rats assessed by a refined procedure of the Hebb-Williams maze task J Neurosci Res 70 2002 340 346
30. C. Kohler, B. Srebro Effects of lateral and medial septal lesions on exploratory behavior in the albino rat Brain Res 182 1980 423 440
31. B. Kolb, M. Forgie, R. Gibb, G. Gorny, S. Rowntree Experience, and the aging brain Neurosci Biobehav Rev 22 1998 143 159
32. T.J. Kornecook, T.E. Kippin, J.P. Pinel Basal forebrain damage and object-recognition in rats Behav Brain Res 98 1999 67 76
33. C. Labelle, N. Leclerc Exogenous BDNF, NT-3 and NT-4 differentially regulate neurite outgrowth in cultured hippocampal neurons Brain Res Dev 123 2000 1 11
34. M.R. Lamprea, F.P. Cardenas, R. Silveira, T.J. Walsh, S. Morato Effects of septal cholinergic lesion on rat exploratory behavior in an open-field Braz J Med Biol Res 36 2003 233 238
35. G. Leanza, O.G. Nilsson, R.G. Wiley, A. Bjorklund 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
36. O. Lehmann, A.J. Grottick, J.C. Cassel, G.A. Higgins A double dissociation between serial reaction time and radial maze performance in rats subjected to 192 IgG-saporin lesions of the nucleus basalis and/or the septal region Eur J Neurosci 18 2003 651 666
37. O. Lehmann, H. Jeltsch, O. Lehnardt, L. Pain, C. Lazarus, J.C. Cassel Combined lesions of cholinergic and serotonergic neurons in the rat brain using 192 IgG-saporin and 5,7-dihydroxytryptamine neurochemical and behavioural characterization Eur J Neurosci 12 2000 67 79
38. P.C. Maisonpierre, L. Belluscio, B. Friedman, R.F. Alderson, S.J. Wiegand, M.E. Furth, R.M. Lindsay, G.D. Yancopoulos NT-3, BDNF, and NGF in the developing rat nervous system parallel as well as reciprocal patterns of expression Neuron 5 1990 501 509
39. J. McGaughy, J.W. Dalley, C.H. Morrison, B.J. Everitt, T.W. Robbins Selective behavioral and neurochemical effects of cholinergic lesions produced by intrabasalis infusions of 192 IgG-saporin on attentional performance in a five-choice serial reaction time task J Neurosci 22 2002 1905 1913
40. J. McGaughy, B.J. Everitt, T.W. Robbins, M. Sarter The role of cortical cholinergic afferent projections in cognition impact of new selective immunotoxins Behav Brain Res 115 2000 251 263
41. J.L. Muir, W. Fischer, A. Björklund Decline in visual attention and spatial memory in aged rats Neurobiol Aging 20 1999 605 615
42. S. Nag, F. Tang Cholinergic lesions of the rat brain by ibotenic acid and 192 IgG-saporin effects on somatostatin, substance P and neuropeptide Y levels in the cerebral cortex and the hippocampus Neurosci Lett 252 1998 83 86
43. H. Nakamura, S. Kobayashi, Y. Ohashi, S. Ando Age-changes of brain synapses and synaptic plasticity in response to an enriched environment J Neurosci Res 56 1999 307 315
44. D. Nonner, E.F. Barrett, J.N. Barrett Neurotrophin effects on survival and expression of cholinergic properties in cultured rat septal neurons under normal and stress conditions J. Neurosci 16 1996 6665 6675
45. J. O'Keef, L. Nadel The hippocampus as a cognitive map 1978 Clarendon Press Oxford, UK
46. D.S. Olton Dementia animal models of the cognitive impairments following damage to the basal forebrain cholinergic system Brain Res Bull 25 1990 499 502
47. M.J. Passineau, E.J. Green, W.D. Dietrich Therapeutic effects of environmental enrichment on cognitive function and tissue integrity following severe traumatic brain injury in rats Exp Neurol 168 2001 373 384
48. G. Paxinos, C. Watson The rat brain in stereotaxic coordinates 4th ed. 1998 Academic Press San Diego
49. T. Perry, H. Hodges, J.A. Gray Behavioural, histological and immunocytochemical consequences following 192 IgG-saporin immunolesions of the basal forebrain cholinergic system Brain Res Bull 54 2001 29 48
50. D.P. Pizzo, V. Paban, N.G. Coufal, F.H. Gage, L.J. Thal Long-term production of choline acetyltransferase in the CNS after transplantation of fibroblasts modified with a regulatable vector Mol Brain Res 126 2004 1 13
51. D.P. Pizzo, L.J. Thal, J. Winkler Mnemonic deficits in animals depend upon the degree of cholinergic deficit and task complexity Exp Neurol 177 2002 292 305
52. D.P. Pizzo, J.J. Waite, L.J. Thal, J. Winkler Intraparenchymal infusions of 192 IgG-saporin development of a method for selective and discrete lesioning of cholinergic basal forebrain nuclei J Neurosci Methods 91 1999 9 19
53. L. Ricceri, C. Hohmann, J. Berger-Sweeney Early neonatal 192 IgG saporin induces learning impairments and disrupts cortical morphogenesis in rats Brain Res 954 2002 160 172
54. R.M. Ridley, H.C. Barefoot, C.J. Maclean, P. Pugh, H.F. Baker Different effects on learning ability after injection of the cholinergic immunotoxin ME20.4IgG-saporin into the diagonal band of Broca, basal nucleus of Meynert, or both in monkeys Behav Neurosci 113 1999 303 315
55. M.R. Rosenzweig Experience, memory, and the brain Am Psychol 39 1984 365 376
56. S. Rossner Cholinergic immunolesions by 192IgG-saporin-useful tool to simulate pathogenic aspects of Alzheimer's disease Int J Dev Neurosci 15 1997 835 850
57. S. Rossner, R. Schliebs, V. Bigl 192IgG-saporin-induced immunotoxic lesions of cholinergic basal forebrain system differentially affect glutamatergic and GABAergic markers in cortical rat brain regions Brain Res 696 1995 165 176
58. S. Saito, S. Kobayashi, Y. Ohashi, M. Igarashi, Y. Komiya, S. Ando Decreased synaptic density in aged brains and its prevention by rearing under enriched environment as revealed by synaptophysin contents J Neurosci Res 39 1994 57 62
59. M. Sarter, J.P. Bruno Cognitive functions of cortical acetylcholine toward a unifying hypothesis Brain Res Rev 23 1997 28 46
60. E.M. Torres, T.A. Perry, A. Blockland, L.S. Wilkinson, R.G. Wiley, D.A. Lappi, S.B. Dunnet Behavioural, histochemical and biochemical consequences of selective immunolesions in discrete regions of the basal forebrain cholinergic system Neuroscience 63 1994 95 122
61. H. Van Praag, G. Kempermann, F.H. Gage Neural consequences of environmental enrichment Nat Rev Neurosci 1 2000 191 198
62. N. Vnek, L.F. Kromer, R.G. Wiley, L.A. Rothblat The basal forebrain cholinergic system and object memory in the rat Brain Res 710 1996 265 270
63. M.L. Voytko, D.S. Olton, R.T. Richardson, L.K. Gorman, J.R. Tobin, D.L. Price Basal forebrain lesions in monkeys disrupt attention but not learning and memory J Neurosci 14 1994 167 186
64. A.K. Wagner, A.E. Kline, J. Sokoloski, R.D. Zafonte, E. Capulong, C.E. Dixon Intervention with environmental enrichment after experimental brain trauma enhances cognitive recovery in male but not female rats Neurosci Lett 334 2002 165 168
65. J.J. Waite, A.D. Chen Differential changes in rat cholinergic parameters subsequent to immunotoxic lesion of the basal forebrain nuclei Brain Res 918 2001 113 120
66. J.J. Waite, A.D. Chen, M.L. Wardlow, L.J. Thal Behavioral and biochemical consequences of combined lesions of the medial septum/diagonal band and nucleus basalis in the rat when ibotenic acid, quisqualic acid, and AMPA are used Exp Neurol 130 1994 214 229
67. J.J. Waite, A.D. Chen, M.L. Wardlow, R.G. Wiley, D.A. Lappi, L.J. Thal 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
68. J.J. Waite, M.L. Wardlow, A.C. Chen, D.A. Lappi, R.G. Wiley, L.J. Thal Time course of cholinergic and monoaminergic changes in rat brain after immunolesioning with 192 IgG-saporin Neurosci Lett 169 1994 154 158
69. T.J. Walsh, C.D. Herzog, C. Gandhi, R.W. Stackman, R.G. Wiley Injection of IgG 192-saporin into the medial septum produces cholinergic hypofunction and dose-dependent working memory deficits Brain Res 726 1996 69 79
70. T.J. Walsh, K.D. Opello Neuroplasticity, the aging brain, and Alzheimer's disease Neurotoxicology 13 1992 101 110
71. G.L. Wenk The nucleus basalis magnocellularis cholinergic system one hundred years of progress Neurobiol Learn Mem 67 1997 85 95
72. G.L. Wenk, J.D. Stoehr, G. Quintana, S. Mobley, R.G. Wiley Behavioral, biochemical, histological, and electrophysiological effects of 192 IgG-saporin injections into the basal forebrain of rats J Neurosci 14 1994 5986 5995
73. P.J. Whitehouse, R.G. Struble, A.W. Clark, D.L. Price Alzheimer disease plaques, tangles, and the basal forebrain Ann Neurol 12 1982 494
74. R.G. Wiley Neural lesioning with ribosome-inactivating proteins suicide transport and immunolesioning Trends Neurosci 15 1992 285 290
75. B.M. Williams, Y. Luo, C. Ward, K. Redd, R. Gibson, S.A. Kuczaj, J.G. McCoy Environmental enrichment effects on spatial memory and hippocampal CREB immunoreactivity Physiol Behav 73 2001 649 658
76. K.T. Winterfeld, G. Teuchert-Noodt, R.R. Dawirs Social environment alters both ontogeny of dopamine innervation of the medial prefrontal cortex and maturation of working memory in gerbils (Meriones unguiculatus) J Neurosci Res 52 1998 201 209
77. C.C. Wrenn, D.A. Lappi, R.G. Wiley Threshold relationship between lesion extent of the cholinergic basal forebrain in the rat and working memory impairment in the radial maze Brain Res 847 1999 284 298
78. C.C. Wrenn, R.G. Wiley The behavioral functions of the cholinergic basal forebrain lessons from 192 IgG-saporin Int J Dev Neurosci 16 1998 595 602