Neonatal 192 IgG-saporin lesion of forebrain cholinergic neurons: Focus on the life span?

Neuroscience and Biobehavioral Reviews

Volumn 27, Issue 4, 2003, Pages 365-376

  Pappas, Bruce A ^a   Sherren, Nicole ^a  

^a CARLETON UNIVERSITY   (Canada)

Author keywords

192 IgG saporin; Acetylcholine; Attention; Dementia; Memory; Norepinephrine; P75NTR; Problem solving; Rett syndrome; Sex differences

Indexed keywords

192 IGG SAPORIN; IMMUNOTOXIN; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; BRAIN CORTEX LESION; BRAIN DYSFUNCTION; BRAIN REGION; CHOLINERGIC SYSTEM; COGNITION; CONFERENCE PAPER; CYTOARCHITECTURE; DENDRITE; DEVELOPMENTAL STAGE; FOREBRAIN; HUMAN; INNERVATION; INTELLIGENCE; LEARNING; MAZE TEST; MEMORY; NERVE CELL DIFFERENTIATION; NERVE CELL LESION; NERVE PROJECTION; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; NORADRENERGIC SYSTEM; PRIORITY JOURNAL; RETT SYNDROME; SEX DIFFERENCE; STATISTICAL SIGNIFICANCE; SYNAPSE;

EID: 0042018737     PISSN: 01497634     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0149-7634(03)00067-8     Document Type: Conference Paper

References (85)

1. Angelleti P.U. Chemical sympathectomy in newborn animals. Neuropharmacology. 10:1971;55-59.
2. Armstrong D.D., Dunn J.K., Antalffy B., Trivedi R. Selective dendritic alterations in the cortex of Rett syndrome. J Neuropathol Exp Neurol. 54:1995;195-201.
3. Armstrong D.D., Dunn K., Antalffy B. Decreased dendritic branching in frontal, motor and limbic cortex in Rett syndrome compared with trisomy 21. J Neuropathol Exp Neurol. 57:1998;1013-1017.
4. Bachman E.S., Berger-Sweeney J., Coyle J.T., Hohmann C.F. Developmental regulation of adult cortical morphology and behavior: an animal model for mental retardation. Int J Dev Neurosci. 12:1994;239-253.
5. Becker L.E., Armstrong D.L., Chan F. Dendritic atrophy in children with Down's syndrome. Ann Neurol. 20:1986;520-526.
6. Belichenko P.V., Oldfors A., Hagberg B., Dahlstrom A. Rett syndrome: 3-D confocal microscopy of cortical pyramidal dendrites and afferents. Neuroreport. 5:1994;1509-1513.
7. Berger-Sweeney J., Heckers S., Mesulam M.-M., Wiley R.G., Lappi D.A., Sharma M. 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. Berger-Sweeney J., Hohmann C.F. Behavioral consequences of abnormal cortical developmental: insights into developmental disabilities. Behav Brain Res. 86:1997;121-142.
9. Berger-Sweeney J. The effects of neonatal basal forebrain lesions on cognition: towards understanding the developmental role of the cholinergic basal forebrain. Int J Dev Neurosci. 16:1998;603-612.
10. Book A.A., Wiley R.G., Schweitzer J.B. Specificity of 192 IgG-saporin for NGF receptor-positive cholinergic basal forebrain neurons in the rat. Brain Res. 590:1992;350-355.
11. Carli M., Robbins T.W., Evenden J.L., Everitt B.J. Effects of lesions to ascending noradrenergic neurones on performance of a 5-choice serial reaction task in rats; implications for theories of dorsal noradrenergic bundle function based on selective attention and arousal. Behav Brain Res. 9:1983;361-380.
12. Casanova M.F., Walker L.C., Whitehouse P.J., Price D. Abnormalities of the nucleus basalis in Down's syndrome. Ann Neurol. 18:1985;310-313.
13. Chen C.-K., Kinsman S.L., Hottzman D.M., Morley W.C., Johnston M.V. A reverse transcription-polymerase chain reaction study of p75 nerve growth factor receptor gene expression in developing rat cerebellum. Int J Dev Neurosci. 12:1994;255-262.
14. Clarke A. Rett syndrome. J Med Genet. 33:1996;693-699.
15. Cordero M.E., Trejo M., Garcia E., Barros T., Rojas A.M., Colombo M. Dendritic development in the neocortex of adult rats following a maintained prenatal and/or early postnatal life undernutrition. Early Hum Dev. 14:1986;245-258.
16. Coyle J.T., Price D.L., DeLong M.R. Alzheimer's disease: a disorder of cortical cholinergic innervation. Science. 219:1983;1184-1190.
17. Coyle J.T., Yamamura H.I. Neurochemical aspects of the ontogenesis of cholinergic neurons in the rat brain. Brain Res. 118:1976;429-440.
18. Coyle J.T., Oster-Granite M.L., Gearhart J.D. The neurobiologic consequences of Down syndrome. Brain Res Bull. 16:1986;773-787.
19. Crutcher K.A. Sympathetic sprouting in the central nervous system: a model for studies of axonal growth in the mature mammalian brain. Brain Res Rev. 12:1987;203-233.
20. Dokla C.P.J., Thal L.J. Effect of cholinesterase inhibitors on Morris water task behavior following lesions of the nucleus basalis magnocellularis. Behav Neurosci. 102:1988;861-871.
21. Dotti M.T., Orrico A., De Stefano N., Battisti C., Sicurelli F., Severi S., Lam C.W., Sorrentino V., Federico A. A Rett syndrome MECP2 mutation that causes mental retardation in men. Neurology. 59:2002;226-230.
22. Dreyfus C.F. Neurotransmitters and neurotrophins collaborate to influence brain development. Perspect Dev Neurobiol. 5:1998;389-399.
23. Eichenbaum H. A cortical-hippocampal system for declarative memory. Nat Rev Neurosci. 1:2000;41-50.
24. Felten D.L., Hallman H., Jonsson G. Evidence for a neurotrophic role of noradrenaline neurons in the postnatal development of rat cerebral cortex. J Neurocytol. 11:1982;119-135.
25. Friedman W.J., Ibáñez C.F., Hallböök F., Persson H., Cain L.D., Drefyus C.F., Black I.B. Differential actions of neurotrophins in the locus coeruleus and basal forebrain. Exp Neurol. 119:1993;72-78.
26. Galani R., Weiss I., Cassel J.C., Kelche C. Spatial memory, habituation, and reactions to spatial and nonspatial changes in rats with selective lesions of the hippocampus, the entorhinal cortex or the subiculum. Behav Brain Res. 96:1998;1-12.
27. Gill T.M., Sarter M., Givens B. Sustained visual attention performance-associated prefrontal neuronal activity: evidence for cholinergic modulation. J Neurosci. 20:2000;4745-4757.
28. Godridge H., Reynolds G.P., Czudek C., Calcutt N.A., Benton M. Alzheimer-like neurotransmitter deficits in adult Down's syndrome brain tissue. J Neurol Neurosurg Psychiatry. 50:1987;775-778.
29. Gutiérrez H., Miranda M.I., Bermúdez-Rattoni F. Learning impairment and cholinergic deafferentation after cortical nerve growth factor deprivation. J Neurosci. 17:1997;3796-3803.
30. Hagberg B. Rett syndrome: clinical peculiarities and biological mysteries. Acta Paediatr. 84:1995;971-976.
31. Heckers S., Ohtake T., Wiley R.G., Lappi D.A., Geula C., Mesulam M.-M. 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.
32. Hepler D.J., Wenk G.L., Cribbs B.L., Olton D.S., Coyle J.T. Memory impairments following basal forebrain lesions. Brain Res. 346:1985;8-14.
33. Hohmann C.F., Brooks A.R., Coyle J.T. Neonatal lesions of the basal forebrain cholinergic neurons result in abnormal cortical development. Dev Brain Res. 42:1988;253-264.
34. Hohmann C.F., Berger-Sweeney J. Sexually dimorphic responses to neonatal basal forebrain lesions in mice: II. Cortical morphology. J Neurobiol. 37:1998;595-606.
35. Houser C.R., Crawford G.D., Salvaterra P.M., Vaughn J.E. Immunocytochemical localization of choline acetyltransferase in rat cerebral cortex: a study of cholinergic neurons and synapses. J Comp Neurol. 234:1985;17-34.
36. Jarrard L.E. On the role of the hippocampus in learning and memory in the rat. Behav Neural Biol. 60:1993;9-26.
37. Kaufmann W.E., Naidu S., Budden S. Abnormal expression of microtubule-associated protein 2 (MAP-2) in neocortex in Rett syndrome. Neuropediatrics. 26:1995;109-113.
38. Kaufmann W.E., Moser H.W. Dendritic abnormalities in disorders associated with mental retardation. Cereb Cortex. 10:2000;981-991.
39. Kiss J., Patel A.J. Development of the cholinergic fibres innervating the cerebral cortex of the rat. Int J Dev Neurosci. 10:1992;153-170.
40. Kitt C.A., Wilcox B.J. Preliminary evidence for neurodegenerative changes in the substantia nigra of Rett syndrome. Neuropediatrics. 26:1995;114-118.
41. Koh S., Loy R. Localization and development of nerve growth factor-sensitive rat basal forebrain neurons and their afferent projections to hippocampus and neocortex. J Neurosci. 9:1989;2999-3018.
42. Kornack D.R., Lu B., Black I.B. Sexually dimorphic expression of the NGF receptor gene in the developing rat brain. Brain Res. 542:1991;171-174.
43. Kostrzewa R.M., Reader T.A., Descarries L. Serotonin neural adaptations to ontogenetic loss of dopamine neurons in rat brain. J Neurochem. 70:1998;889-898.
44. Lauder J.M. Neurotransmitters as growth regulatory signals: role of receptors and second messengers. Trends Neurosci. 16:1993;233-240.
45. Leanza G., Nilsson O.G., Wiley R.G., Bjorklund 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.
46. Leanza G., Nilsson O.G., Nikkhah G., Wiley R.G., Bjorklund A. Effects of neonatal lesions of the basal forebrain cholinergic system by 192 immunoglobulin G-saporin: biochemical, behavioural and morphological characterization. Neuroscience. 74:1996;119-141.
47. Lipani J.D., Bhattacharjee M.B., Corey D.M., Lee D.A. Reduced nerve growth factor in Rett syndrome postmortem brain tissue. J Neuropathol Exp Neurol. 59:(10):2000;889-895.
48. Loy R., Sheldon R.A. Sexually dimorphic development of cholinergic enzymes in the rat septohippocampal system. Dev Brain Res. 34:1987;156-160.
49. Lubec B., Yoo B.C., Dierssen M., Balic N., Lubec G. Down syndrome patients start early prenatal life with normal cholinergic, monoaminergic and serotonergic innervation. J Neural Transm Suppl. 61:2001;303-310.
50. Mann D.M.A., Yates P.O., Marcyniuk B. Dopaminergic neurotransmitter systems in Alzheimer's disease and in Down's syndrome at middle age. J Neurol Neurosurg Psychiatry. 50:1987;341-344.
51. Mann D.M.A., Brown A., Prinja D., Davies C.A., Landon M., Masters C.L., Beyreuther K. An analysis of the morphology of senile plaques in Down's syndrome patients of different ages using immunocytochemical and lectin histochemical techniques. Neuropathol Appl Neurobiol. 15:1989;317-329.
52. Markowska A.L., Wenk G.L., Olton D.S. Nucleus basalis magnocellularis and memory: differential effects of two neurotoxins. Behav Neural Biol. 54:1990;13-26.
53. Mattsson A., Ögren S.O., Olson L. Facilitation of dopamine-mediated locomotor activity in adult rats following cholinergic denervation. Exp Neurol. 174:2002;96-108.
54. McGaughy J., Kaiser T., Sarter M. Behavioral vigilance following infusions of 192 IgG-saporin into the basal forebrain: selectivity of the behavioral impairment and relation to cortical AChE-positive fiber density. Behav Neurosci. 110:1996;247-265.
55. McGaughy J., Sarter M. Sustained attention performance in rats with intracortical infusions of 192 IgG-saporin-induced cholinergic deafferentation: effects of physostigmine and FG 7142. Behav Neurosci. 112:1998;1519-1525.
56. Mrzljak L., Pappy M., Leranth C., Goldman-Rakic P.S. Cholinergic synaptic circuitry in the macaque prefrontal cortex. J Comp Neurol. 357:1995;603-617.
57. Murray C.L., Fibiger H.C. Learning and memory deficits after lesions of the nucleus basalis magnocellularis: reversal by physostigmine. Neuroscience. 14:1985;1025-1032.
58. Pappas B.A., Davidson C.M., Fortin T., Nallathamby S., Park G.A.S., Mohr E., Wiley R.G. 192 IgG-saporin lesion of basal forebrain cholinergic neurons in neonatal rats. Dev Brain Res. 96:1996;52-61.
59. Pappas B.A., Nguyen T., Brownlee B., Tanasoiu D., Fortin T., Sherren N. Ectopic noradrenergic hyperinnervation does not functionally compensate for neonatal forebrain acetylcholine lesion. Brain Res. 867:2000;90-99.
60. Peters D.A.V., Mazurkiewicz-Kwilecki I.M., Pappas B.A. 6-hydoxydopamine sympathectomy in the neonatal rat-effects on brain serotonin and histamine. Biochem Pharmacol. 23:1974;2395-2401.
61. Reiss A.L., Faruque F., Naidu S., Abrams M., Beaty T., Bryan R.N., Moser H. Neuroanatomy of Rett syndrome: a volumetric imaging study. Ann Neurol. 34:1993;227-234.
62. Ricceri L., Calamandrei G., Berger-Sweeney J. Different effects of postnatal day 1 versus 7 192 immunoglobulin G-saporin lesions on learning, exploratory behaviors, and neurochemistry in juvenile rats. Behav Neurosci. 111:1997;1292-1302.
63. Ricceri L., Hohmann C., Berger-Sweeney J. Early neonatal 102 IgG saporin induces learning impairments and disrupts cortical morphogenesis in rats. Brain Res. 954:2002;160-172.
64. Robertson R.T., Gallardo K.A., Claytor K.J., Ha D.H., Ku K.-H., Yu B.P., Lauterborn J.C., Wiley R.G., Yu J., Gall C.M., Leslie F.M. Neonatal treatment with 192 IgG-saporin produces long-term forebrain cholinergic deficits and reduces dendritic branching and spine density of neocortical pyramidal neurons. Cereb Cortex. 8:1998;142-155.
65. Roβner S., Schliebs R., Härtig W., Bigl V. 192 IgG-saporin-induced selective lesion of cholinergic basal forebrain system: neurochemical effects on cholinergic neurotransmission in rat cerebral cortex and hippocampus. Brain Res Bull. 38:1995;371-381.
66. Schwartz J.P. Neurotransmitters as neurotrophic factors: a new set of functions. Int Rev Neurobiol. 34:1992;1-23.
67. Sengstock G.J., Johnson K.B., Jantzen P.T., Meyer E.M., Dunn A.J., Arendash G.W. Nucleus basalis lesions in neonate rats induce a selective cortical cholinergic hypofunction and cognitive deficits during adulthood. Exp Brain Res. 90:1992;163-174.
68. Shastry B.S. Molecular genetics of Rett syndrome. Neurochem Int. 38:2001;503-508.
69. Sherren N., Pappas B.A., Fortin T. Neural and behavioral effects of intracranial 192 IgG-saporin in neonatal rats: sexually dimorphic effects? Dev Brain Res. 114:1999;49-62.
70. Snowdon D.A., Kemper S.J., Mortimer J.A., Greiner L.H., Wekstein D.R., Markesbery W.R. Linguistic ability in early life and cognitive function and Alzheimer's disease in later life: findings from the Nun study. J Am Med Assoc. 275:1996;528-532.
71. Squire L.R. Memory systems. C R Acad Sci III. 321:1998;153-156.
72. 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.
73. Subramaniam B., Naidu S., Reiss A.L. Neuroanatomy in Rett syndrome: cerebral cortex and posterior fossa. Neurology. 48:1997;399-407.
74. Takashima S., Becker L.E., Armstrong D.L., Chan F. Abnormal neuronaldevelopment in the visual cortex of the human fetus and infant with Down's syndrome. A quantitative and qualitative Golgi study. Brain Res. 225:1981;1-21.
75. Terry R.D., Katzman R. Life span and synapses: will there be a primary senile dementia? Neurobiol Aging. 22:2001;347-348.
76. Turchi J., Sarter M. Cortical cholinergic inputs mediate processing capacity: effects of 192 IgG-saporin-induced lesions on olfactory span performance. Eur J Neurosci. 12:2000;4505-4514.
77. Villard L., Kpebe A., Cardoso C., Chelly J., Tardieu M., Fontes M. Two affected boys in a Rett syndrome family. Neurology. 55:2000;1188-1193.
78. Waite J.J., Wardlow M.L., Chen A.C., Lappi D.A., Wiley R.G., Thal L.J. Time course of cholinergic and monoaminergic changes in rat brain after immunolesioning with 192 IgG-saporin. Neurosci Lett. 169:1994;154-158.
79. Waite J.J., Wardlow M.L., Power A.E. Deficit in selective and divided attention associated with cholinergic basal forebrain immunotoxic lesion produced by 192-saporin; motoric/sensory deficit associated with purkinje cell immunotoxic lesion produced by OX7-saporin. Neurobiol Learn Mem. 71:1999;325-352.
80. Walsh T.J., Kelly R.M., Dougherty K.D., Stackman R.W., Wiley R.G., Kutscher C.L. Behavioral and neurobiological alterations induced by the immunotoxin 192-IgG-saporin: cholinergic and non-cholinergic effects following i.c.v. injection. Brain Res. 702:1995;233-245.
81. Weiss B. The behavioral toxicology of metals. Fed Proc. 37:1978;22-27.
82. Wenk G.L. Rett syndrome: neurobiological changes underlying specific symptoms. Prog Neurobiol. 51:1997;383-391.
83. Wenk G.L., Hauss-Wegrzyniak B. Altered cholinergic function in the basal forebrain of girls with Rett syndrome. Neuropediatrics. 30:1999;125-129.
84. Wenk G.L., Naidu S., Casanova M.F., Kitt C.A., Moser H. Altered neurochemical markers in Rett's syndrome. Neurology. 41:1991;1753-1756.
85. 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.