Does age matter? behavioral and neuro - Anatomical effects of neonatal and adult basal forebrain cholinergic lesions

Journal of Alzheimer's Disease

Volumn 20, Issue 1, 2010, Pages 207-227

  De Bartolo, Paola ^a,b   Cutuli, Debora ^a,b   Ricceri, Laura ^c   Gelfo, Francesca ^a,d   Foti, Francesca ^a,b   Laricchiuta, Daniela ^a,b   Scattoni, Maria Luisa ^c   Calamandrei, Gemma ^c   Petrosini, Laura ^a,b  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^d UNIVERSITY OF NAPLES PARTHENOPE   (Italy)

Author keywords

192 IgG saporin; Age effect; Alzheimer's disease; cholinergic lesion; neuronal morphology; pyramidal neurons; rat; spatial function

Indexed keywords

SAPORIN;

AGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; CONTROLLED STUDY; DENDRITIC SPINE; FEMALE; MALE; MAZE TEST; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SPATIAL DISCRIMINATION;

EID: 77954494783     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2010-1355     Document Type: Article

References (109)

1. Perry EK, Perry RH, Gibson PH, Blessed G, Tomlinson BE (1977) A cholinergic connection between normal aging and senile dementia in the human hippocampus. Neurosci Lett 6, 85-89.
2. Sarter M, Bruno JP (2004) Developmental origins of the agerelated decline in cortical cholinergic function and associated cognitive abilities. Neurobiol Aging 25, 1127-1139.
3. Nordberg A (2006) Mechanisms behind the neuroprotective actions of cholinesterase inhibitors in Alzheimer disease. Alzheimer Dis Assoc Disord 20, S12-S18.
4. Davies P, Maloney AJ (1976) Selective loss of central cholinergic neurons in Alzheimer's disease. Lancet 2, 1403.
5. Birks J, Flicker L (2006) Donepezil for mild cognitive impairment. Cochrane Database Syst Rev 3, CD006104.
6. Bartus RT, Dean RL III, Beer B, Lippa AS (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217, 408-414.
7. Bartus RT (2000) On neurodegenerative diseases, models, and treatment strategies: lessons learned and lessons forgotten a generation following the cholinergic hypothesis. Exp Neurol 163, 495-529.
8. Freo U, Pizzolato G,DamM, Ori C, BattistinL(2002)Ashort review of cognitive and functional neuroimaging studies of cholinergic drugs: implications for therapeutic potentials. J Neural Transm 109, 857-870.
9. Sarter M, Bruno JP, Givens B (2003) Attentional functions of cortical cholinergic inputs: what does it mean for learning and memory? Neurobiol Learn Mem 80, 245-256.
10. Phillis JW (2005) Acetylcholine release from the central nervous system: a 50-year retrospective. Crit Rev Neurobiol 17, 161-217.
11. Mufson EJ, Deecher DC, Basile M, Izenwasse S, Mash DC (2000) Galanin receptor plasticity within the nucleus basalis in early and late Alzheimer's disease: an in vitro autoradiographic analysis. Neuropharmacology 39, 1404-1412.
12. Mufson EJ, Ma SY, Dills J, Cochran EJ, Leurgans S, Wuu J, Bennett DA, Jaffar S, Gilmor ML, Levey AI, Kordower JH (2002) Loss of basal forebrain P75(NTR) immunoreactivity in subjects with mild cognitive impairment and Alzheimer's disease. J Comp Neurol 443, 136-153.
13. Nilsson OG, Leanza G, Rosenblad C, Lappi DA, Wiley RG, Bjorklund A (1992) Spatial learning impairments in rats with selective immunolesion of the forebrain cholinergic system. Neuroreport 3, 1005-1008.
14. Wenk GL, Stoehr JD, Quintana G, Mobley S, Wiley RG (1994) Behavioral, biochemical, histological, and electrophysiological effects of 192 IgG-saporin injections into the basal forebrain of rats. J Neurosci 14, 5986-5995.
15. Baxter MG, Bucci DJ, Gorman LK, Wiley RG, Gallagher M (1995) Selective immunotoxic lesions of basal forebrain cholinergic cells: effects on learning and memory in rats. Behav Neurosci 109, 714-722.
16. Waite JJ, Thal LJ (1996) Lesions of the cholinergic nuclei in the rat basal forebrain: excitotoxins vs. an immunotoxin. Life Sci 58, 1947-1953.
17. Leanza G, Nilsson OG, Nikkhah G, Wiley RG, Bjorklund A (1996) Effects of neonatal lesions of the basal forebrain cholinergic system by 192 immunoglobulin G-saporin: biochemical, behavioural and morphological characterization. Neuroscience 74, 119-141.
18. Rossner S (1997) Cholinergic immunolesions by 192IgGsaporin-useful tool to simulate pathogenic aspects of Alzheimer's disease. Int J Dev Neurosci 15, 835-850.
19. Wrenn CC, Wiley RG (2001) Lack of effect of moderate Purkinje cell loss on working memory. Neuroscience 107, 433-445.
20. Torres EM, Perry TA, Blockland A,Wilkinson LS,Wiley RG, Lappi DA, Dunnet SB (1994) Behavioural, histochemical and biochemical consequences of selective immunolesions in discrete regions of the basal forebrain cholinergic system. Neuroscience 63, 95-122.
21. Lehmann O, Jeltsch H, Lehnardt O, Pain L, Lazarus C, Cassel JC (2000) 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, 67-79.
22. Lehmann O, Bertrand F, Jeltsch H, Morer M, Lazarus C,Will B, Cassel JC (2002) 5,7-DHT-induced hippocampal 5-HT depletion attenuates behavioural deficits produced by 192 IgG-saporin lesions of septal cholinergic neurons in the rat. Eur J Neurosci 15, 1991-2006.
23. Galani R, Jeltsch H, Lehmann O, Bertrand F, Cassel J C (2002) Effects of 192 IgG-saporin on acetylcholinesterase histochemistry in male and female rats. Brain Res Bull 58, 179-186.
24. Leanza G, Nilsson OG, Wiley RG, Bjorklund 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.
25. Waite JJ, Chen AD,Wardlow ML,Wiley RG, Lappi DA, Thal LJ (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.
26. Walsh TJ, Kelly RM, Dougherty KD, Stackman RW, Wiley RG, Kutscher CL (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.
27. Wiley RG, Berbos TG, Deckwerth TL, JohnsonEMJr., Lappi DA (1995) Destruction of the cholinergic basal forebrain using immunotoxin to rat NGF receptor: modeling the cholinergic degeneration of Alzheimer's disease. J Neurol Sci 128, 157-166.
28. Ricceri L, Calamandrei G, Berger-Sweeney J (1997) 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, 1292-1302.
29. Ricceri L, Usiello A, Valanzano A, Calamandrei G, Frick K, Berger-Sweeney J (1999) Neonatal 192 IgG-saporin lesions of basal forebrain cholinergic neurons selectively impair response to spatial novelty in adult rats. Behav Neurosci 113, 1204-1215.
30. Ricceri L (2003) Behavioral patterns under cholinergic control during development: lessons learned from the selective immunotoxin 192 IgG saporin. Neurosci Biobehav Rev 27, 377-384.
31. Robertson RT, Gallardo KA, Claytor KJ, Ha DH, Ku KH, Yu BP, Lauterborn JC, Wiley RG, Yu J, Gall CM, Leslie FM (1998) 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, 142-155.
32. Ricceri L, Hohmann C, Berger-Sweeney J (2002) Early neonatal 192 IgG saporin induces learning impairments and disrupts cortical morphogenesis in rats. Brain Res 954, 160-172.
33. Lauder JM, Schambra UB (1999) Morphogenetic roles of acetylcholine. Environ Health Perspect 107(Suppl 1), 65-69.
34. Ricceri L, Minghetti L, Moles A, Popoli P, Confaloni A, De Simone R, Piscopo P, Scattoni ML, di Luca M, Calamandrei G(2004) Cognitive and neurological deficits induced by early and prolonged basal forebrain cholinergic hypofunction in rats. Exp Neurol 189, 162-172.
35. Scattoni ML, Adriani W, Calamandrei G, Laviola G, Ricceri L (2006) Long-term effects of neonatal basal forebrain cholinergic lesions on radial maze learning and impulsivity in rats. Behav Pharmacol 17, 517-524.
36. Harmon KM, Wellman CL (2003) Differential effects of cholinergic lesions on dendritic spines in frontal cortex of young adult and aging rats. Brain Res 992, 60-68.
37. Works SJ, Wilson RE, Wellman CL (2004) Age-dependent effect of cholinergic lesion on dendritic morphology in rat frontal cortex. Neurobiol Aging 25, 963-974.
38. Mandolesi L, De Bartolo P, Foti F, Gelfo F, Federico F, Leggio MG, Petrosini L (2008) Environmental enrichment provides a cognitive reserve to be spent in the case of brain lesion. J Alzheimers Dis 15, 11-28.
39. De Bartolo P, Gelfo F, Mandolesi L, Foti F, Cutuli D, Petrosini L (2009) Effects of chronic donepezil treatment and cholinergic deafferentation on parietal pyramidal neuron morphology. J Alzheimers Dis 17, 177-191.
40. Sherren N, Pappas BA (2005) Selective acetylcholine and dopamine lesions in neonatal rats produce distinct patterns of cortical dendritic atrophy in adulthood. Neuroscience 136, 445-456.
41. Thor DH, Holloway WR Jr. (1986) Social play soliciting by male and female juvenile rats: effects of neonatal androgenization and sex of cagemates. Behav Neurosci 100, 275-279.
42. Paxinos G, Tork I (1990) Neuroanatomical nomenclature. Trends Neurosci 13, 169.
43. Morris RG, Garrud P, Rawlins JN, O'Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297, 681-683.
44. Petrosini L, Molinari M, Dell'Anna ME (1996) Cerebellar contribution to spatial event processing: Morris water maze and T-maze. Eur J Neurosci 8, 1882-1896.
45. Leggio MG, Mandolesi L, Federico F, Spirito F, Ricci B, Gelfo F, Petrosini L (2005) Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behav Brain Res 163, 78-90.
46. Federico F, Leggio MG, Neri P, Mandolesi L, Petrosini L (2006)NMDAreceptor activity in learning spatial procedural strategies II. The influence of cerebellar lesions. Brain Res Bull 70, 356-367. (Pubitemid 44486557)
47. Mandolesi L, Leggio MG, Graziano A, Neri P, Petrosini L (2001) Cerebellar contribution to spatial event processing: involvement in procedural and working memory components. Eur J Neurosci 14, 2011-2022.
48. Molinari M, Grammaldo LG, Petrosini L (1997) Cerebellar contribution to spatial event processing: right/left discrimination abilities in rats. Eur J Neurosci 9, 1986-1992.
49. Jiang X, Johnson RR, Burkhalter A (1993) Visualization of dendritic morphology of cortical projection neurons by retrograde axonal tracing. J Neurosci Methods 50, 45-60.
50. Mesulam MM, Mufson EJ, Wainer BH, Levey AI (1983) Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10, 1185-1201.
51. Gelfo F, De Bartolo P, Giovine A, Petrosini L, Leggio MG (2009) Layer and regional effects of environmental enrichment on the pyramidal neuron morphology of the rat. Neurobiol Learn Mem 91, 353-365.
52. Peters A, Kaiserman-Abramof IR (1970) The small pyramidal neuron of the rat cerebral cortex. The perikaryon, dendrites and spines. Am J Anat 127, 321-355.
53. DeFelipe J, Farinas I (1992) The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs. Prog Neurobiol 39, 563-607.
54. Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82, 239-259.
55. Auld DS, Kornecook TJ, Bastianetto S, Quirion R (2002) Alzheimer's disease and the basal forebrain cholinergic system: relations to beta-amyloid peptides, cognition, and treatment strategies. Prog Neurobiol 68, 209-245.
56. Terry AV Jr., Buccafusco JJ (2003) The cholinergic hypothesis of age and Alzheimer's disease-related cognitive deficits: recent challenges and their implications for novel drug development. J Pharmacol Exp Ther 306, 821-827.
57. Fisher A, Hanin I (1986) Potential animal models for senile dementia of Alzheimer's type, with emphasis on AF64Ainduced cholinotoxicity. Annu Rev Pharmacol Toxicol 26, 161-181.
58. Pepeu G, Giovannini M G (2004) Changes in acetylcholine extracellular levels during cognitive processes. Learn Mem 11, 21-27.
59. Pappas BA, Davidson CM, Fortin T, Nallathamby S, Park GA, Mohr E, Wiley RG (1996) 192 IgG-saporin lesion of basal forebrain cholinergic neurons in neonatal rats. Brain Res Dev Brain Res 96, 52-61.
60. Waite JJ, Wardlow ML, Power AE (1999) 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 byOX7-saporin.Neurobiol LearnMem 71, 325-352.
61. Cutuli D, Foti F, Mandolesi L, De Bartolo P, Gelfo F, Federico F, Petrosini L (2009) Cognitive performances of cholinergically depleted rats following chronic donepezil administration. J Alzheimers Dis 17, 161-176.
62. Cohen-Cory S, Dreyfus CF, Black IB (1989) Expression of high-and low-affinity nerve growth factor receptors by Purkinje cells in the developing rat cerebellum. Exp Neurol 105, 104-109.
63. Buhot MC, Rage P, Segu L (1989) Changes in exploratory behaviour of hamsters following treatment with 8-hydroxy-2-(di-n-propylamino)tetralin. Behav Brain Res 35, 163-179.
64. Save E, Poucet B, Foreman N, Buhot MC (1992) Object exploration and reactions to spatial and nonspatial changes in hooded rats following damage to parietal cortex or hippocampal formation. Behav Neurosci 106, 447-456.
65. Bussey TJ, Saksida LM (2005) Object memory and perception in the medial temporal lobe: an alternative approach. Curr Opin Neurobiol 15, 730-737.
66. Everitt BJ, Robbins TW (1997) Central cholinergic systems and cognition. Annu Rev Psychol 48, 649-684.
67. McMahan RW, Sobel TJ, Baxter MG (1997) Selective immunolesions of hippocampal cholinergic input fail to impair spatial working memory. Hippocampus 7, 130-136.
68. Gilad GM (1987) The stress-induced response of the septohippocampal cholinergic system. A vectorial outcome of psychoneuroendocrinological interactions. Psychoneuroendocrinology 12, 167-184.
69. Mizuno T, Kimura F (1997) Attenuated stress response of hippocampal acetylcholine release and adrenocortical secretion in aged rats. Neurosci Lett 222, 49-52.
70. Mizoguchi K, Yuzurihara M, Ishige A, Sasaki H, Tabira T (2001) Effect of chronic stress on cholinergic transmission in rat hippocampus. Brain Res 915, 108-111.
71. Wrenn CC, Lappi DA,Wiley RG (1999) Threshold relationship between lesion extent of the cholinergic basal forebrain in the rat andworking memory impairment in the radial maze. Brain Res 847, 284-298.
72. Lehmann O, Grottick AJ, Cassel JC, Higgins GA (2003) 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, 651-666.
73. Antonini V, Prezzavento O, Coradazzi M, Marrazzo A, Ronsisvalle S, Arena E, Leanza G (2009) Anti-amnesic properties of (+/-)-PPCC, a novel sigma receptor ligand, on cognitive dysfunction induced by selective cholinergic lesion in rats. J Neurochem 109, 744-754.
74. Pappas BA, Nguyen T, Brownlee B, Tanasoiu D, Fortin T, Sherren N (2000) Ectopic noradrenergic hyperinnervation does not functionally compensate for neonatal forebrain acetylcholine lesion. Brain Res 867, 90-99.
75. Pappas BA, Payne KB, Fortin T, Sherren N (2005) Neonatal lesion of forebrain cholinergic neurons: further characterization of behavioral effects and permanency. Neuroscience 133, 485-492.
76. Steckler T, Keith AB, Wiley RG, Sahgal A (1995) Cholinergic lesions by 192 IgG-saporin and short-term recognition memory: role of the septohippocampal projection. Neuroscience 66, 101-114.
77. Nakamura S, Ishihara T (1990) Task-dependent memory loss and recovery following unilateral nucleus basalis lesion: behavioral and neurochemical correlation. Behav Brain Res 39, 113-122.
78. Gold PE (2003) Acetylcholine modulation of neural systems involved in learning and memory. Neurobiol Learn Mem 80, 194-210.
79. Gill TM, Sarter M, Givens B (2000) Sustained visual attention performance-associated prefrontal neuronal activity: evidence for cholinergic modulation. J Neurosci 20, 4745-4757.
80. McGaughy J, Kaiser T, Sarter M(1996) 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, 247-265.
81. Baxter MG, Holland PC, Gallagher M (1997) Disruption of decrements in conditioned stimulus processing by selective removal of hippocampal cholinergic input. J Neurosci 17, 5230-5236.
82. Stoehr JD, Mobley SL, Roice D, Brooks R, Baker LM,Wiley RG, Wenk G L (1997) The effects of selective cholinergic basal forebrain lesions and aging upon expectancy in the rat. Neurobiol Learn Mem 67, 214-227.
83. Chappell J, McMahan R, Chiba A, Gallagher M(1998) A reexamination of the role of basal forebrain cholinergic neurons in spatial working memory. Neuropharmacology 37, 481-487.
84. Sarter M, Givens B, Bruno JP (2001) The cognitive neuroscience of sustained attention: where top-down meets bottom-up. Brain Res Brain Res Rev 35, 146-160.
85. Kolb B, Forgie M, Gibb R, Gorny G, Rowntree S (1998) Age, experience and the changing brain. Neurosci Biobehav Rev 22, 143-159.
86. Kolb B, Gorny G, Soderpalm AH, Robinson TE (2003) Environmental complexity has different effects on the structure of neurons in the prefrontal cortex versus the parietal cortex or nucleus accumbens. Synapse 48, 149-153.
87. Seib LM, Wellman CL (2003) Daily injections alter spine density in rat medial prefrontal cortex. Neurosci Lett 337, 29-32.
88. Sarti F, Borgland SL, Kharazia VN, Bonci A (2007) Acute cocaine exposure alters spine density and long-term potentiation in the ventral tegmental area. Eur J Neurosci 26, 749-756.
89. Teskey GC, Hutchinson JE, Kolb B (2001) Cortical layer III pyramidal dendritic morphology normalizes within 3 weeks after kindling and is dissociated from kindling-induced potentiation. Brain Res 911, 125-133.
90. Adkins DL, Bury SD, Jones TA (2002) Laminar-dependent dendritic spine alterations in the motor cortex of adult rats following callosal transection and forced forelimb use. Neurobiol Learn Mem 78, 35-52.
91. Gonzalez CL, Kolb B (2003) A comparison of different models of stroke on behaviour and brain morphology. Eur J Neurosci 18, 1950-1962.
92. Schubert D, Kotter R, Zilles K, Luhmann HJ, Staiger JF (2003) Cell type-specific circuits of cortical layer IV spiny neurons. J Neurosci 23, 2961-2970.
93. Rall W(1967) Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. J Neurophysiol 30, 1138-1168.
94. Rall W, Burke RE, Smith TG, Nelson PG, Frank K (1967) Dendritic location of synapses and possible mechanisms for the monosynaptic EPSP in motoneurons. J Neurophysiol 30, 1169-1193.
95. Williams SR, Stuart GJ (2003) Role of dendritic synapse location in the control of action potential output. Trends Neurosci 26, 147-154.
96. Gulledge AT, Kampa BM, Stuart GJ (2005) Synaptic integration in dendritic trees. J Neurobiol 64, 75-90.
97. Berger-Sweeney J (1998) The effects of neonatal basal forebrain lesions on cognition: towards understanding the developmental role of the cholinergic basal forebrain. Int J Dev Neurosci 16, 603-612.
98. Hohmann CF, Berger-Sweeney J (1998) Cholinergic regulation of cortical development and plasticity. New twists to an old story. Perspect Dev Neurobiol 5, 401-425.
99. Mechawar N, Descarries L (2001) The cholinergic innervation develops early and rapidly in the rat cerebral cortex: a quantitative immunocytochemical study. Neuroscience 108, 555-567.
100. Bachman ES, Berger-Sweeney J, Coyle JT, Hohmann CF (1994) Developmental regulation of adult cortical morphology and behavior: an animal model for mental retardation. Int J Dev Neurosci 12, 239-253.
101. Zhu XO, Waite PM (1998) Cholinergic depletion reduces plasticity of barrel field cortex. Cereb Cortex 8, 63-72.
102. Mechawar N, Watkins KC, Descarries L (2002) Ultrastructural features of the acetylcholine innervation in the developing parietal cortex of rat. J Comp Neurol 443, 250-258.
103. Hohmann CF (2003) A morphogenetic role for acetylcholine in mouse cerebral neocortex. Neurosci Biobehav Rev 27, 351-363.
104. Aramakis VB, Hsieh CY, Leslie FM, Metherate R (2000) A critical period for nicotine-induced disruption of synaptic development in rat auditory cortex. J Neurosci 20, 6106-6116.
105. Tremblay N, Warren RA, Dykes RW (1990) Electrophysiological studies of acetylcholine and the role of the basal forebrain in the somatosensory cortex of the cat. I. Cortical neurons excited by glutamate. J Neurophysiol 64, 1199-1211. (Pubitemid 20338962)
106. Tremblay N, Warren RA, Dykes RW (1990) Electrophysiological studies of acetylcholine and the role of the basal forebrain in the somatosensory cortex of the cat. II. Cortical neurons excited by somatic stimuli. J Neurophysiol 64, 1212-1222. (Pubitemid 20338963)
107. Eriksson P, Talts U (2000) Neonatal exposure to neurotoxic pesticides increases adult susceptibility: a review of current findings. Neurotoxicology 21, 37-47.
108. Slotkin TA (2004) Cholinergic systems in brain development and disruption by neurotoxicants: nicotine, environmental tobacco smoke, organophosphates. Toxicol Appl Pharmacol 198, 132-151.
109. Pappas BA, Sherren N (2003) Neonatal 192 IgG-saporin lesion of forebrain cholinergic neurons: focus on the life span? Neurosci Biobehav Rev 27, 365-376.