Selective cholinergic depletion in medial septum leads to impaired long term potentiation and glutamatergic synaptic currents in the hippocampus

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Kanju, Patrick M ^a,b   Parameshwaran, Kodeeswaran ^a   Sims Robinson, Catrina ^a,c   Uthayathas, Subramaniam ^a,d   Josephson, Eleanor M ^a   Rajakumar, Nagalingam ^e   Dhanasekaran, Muralikrishnan ^a   Suppiramaniam, Vishnu ^a  

^a AUBURN UNIVERSITY   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; IMMUNOTOXIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; SAPONIN; SODIUM CHLORIDE; 192 IGG SAPORIN; 192 IGG-SAPORIN; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; CHOLINERGIC RECEPTOR STIMULATING AGENT; MONOCLONAL ANTIBODY; RIBOSOME INACTIVATING PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; BRAIN SYNAPTOSOME; CHOLINERGIC NERVE CELL; CHOLINERGIC SYNAPSE; CHOLINERGIC TRANSMISSION; CONTROLLED STUDY; FEMALE; HIPPOCAMPAL CA1 REGION; LONG TERM POTENTIATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN INDUCTION; PYRAMIDAL NERVE CELL; RAT; STEREOTACTIC PROCEDURE; SYNAPTIC POTENTIAL; ANIMAL; DRUG EFFECT; ENZYME IMMUNOASSAY; EVOKED RESPONSE; INJURY; METABOLISM; PHYSIOLOGY; SEPTUM PELLUCIDUM; SPRAGUE DAWLEY RAT; SYNAPTIC TRANSMISSION; SYNAPTOSOME;

RATTUS; RODENTIA;

ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; ANTIBODIES, MONOCLONAL; CA1 REGION, HIPPOCAMPAL; CHOLINERGIC AGENTS; CHOLINERGIC NEURONS; EVOKED POTENTIALS; FEMALE; IMMUNOENZYME TECHNIQUES; LONG-TERM POTENTIATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; RIBOSOME INACTIVATING PROTEINS, TYPE 1; SEPTUM OF BRAIN; SYNAPTIC TRANSMISSION; SYNAPTOSOMES;

EID: 84857090387     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031073     Document Type: Article

References (101)

1. MacDonald JF, Jackson MF, Beazely MA, (2006) Hippocampal long-term synaptic plasticity and signal amplification of NMDA receptors. Crit Rev Neurobiol 18: 71-84.
2. Malenka RC, (2003) Synaptic plasticity and AMPA receptor trafficking. Ann N Y Acad Sci 1003: 1-11.
3. Maren S, Tocco G, Standley S, Baudry M, Thompson RF, (1993) Postsynaptic factors in the expression of long-term potentiation (LTP): increased glutamate receptor binding following LTP induction in vivo. Proc Natl Acad Sci U S A 90: 9654-9658.
4. Ambros-Ingerson J, Lynch G, (1993) Channel gating kinetics and synaptic efficacy: a hypothesis for expression of long-term potentiation. Proc Natl Acad Sci U S A 90: 7903-7907.
5. Benfenati F, (2007) Synaptic plasticity and the neurobiology of learning and memory. Acta Biomed 78 (Suppl 1): 58-66.
6. Bizon JL, Han JS, Hudon C, Gallagher M, (2003) Effects of hippocampal cholinergic deafferentation on learning strategy selection in a visible platform version of the water maze. Hippocampus 13: 676-684.
7. Benke TA, Luthi A, Isaac JT, Collingridge GL, (1998) Modulation of AMPA receptor unitary conductance by synaptic activity. Nature 393: 793-797.
8. Holmes WR, Grover LM, (2006) Quantifying the magnitude of changes in synaptic level parameters with long-term potentiation. J Neurophysiol 96: 1478-1491.
9. Amaral DG, Kurz J, (1985) An analysis of the origins of the cholinergic and noncholinergic septal projections to the hippocampal formation of the rat. J Comp Neurol 240: 37-59.
10. Araujo DM, Lapchak PA, Robitaille Y, Gauthier S, Quirion R, (1988) Differential alteration of various cholinergic markers in cortical and subcortical regions of human brain in Alzheimer's disease. J Neurochem 50: 1914-1923.
11. Bartus RT, Dean RL 3rd, Beer B, Lippa AS, (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217: 408-414.
12. Bartus RT, Flicker C, Dean RL, Pontecorvo M, Figueiredo JC, et al. (1985) Selective memory loss following nucleus basalis lesions: long term behavioral recovery despite persistent cholinergic deficiencies. Pharmacol Biochem Behav 23: 125-135.
13. Easton A, Fitchett AE, Eacott MJ, Baxter MG, (2010) Medial septal cholinergic neurons are necessary for context-place memory but not episodic-like memory. Hippocampus.
14. Everitt BJ, Robbins TW, (1997) Central cholinergic systems and cognition. Annu Rev Psychol 48: 649-684.
15. Hasselmo ME, (2006) The role of acetylcholine in learning and memory. Curr Opin Neurobiol 16: 710-715.
16. Navakkode S, Korte M, (2011) Cooperation between cholinergic and glutamatergic receptors are essential to induce BDNF-dependent long-lasting memory storage. Hippocampus.
17. Auerbach JM, Segal M, (1994) A novel cholinergic induction of long-term potentiation in rat hippocampus. J Neurophysiol 72: 2034-2040.
18. Blitzer RD, Gil O, Landau EM, (1990) Cholinergic stimulation enhances long-term potentiation in the CA1 region of rat hippocampus. Neurosci Lett 119: 207-210.
19. Kenney JW, Gould TJ, (2008) Modulation of hippocampus-dependent learning and synaptic plasticity by nicotine. Mol Neurobiol 38: 101-121.
20. Mansvelder HD, Mertz M, Role LW, (2009) Nicotinic modulation of synaptic transmission and plasticity in cortico-limbic circuits. Semin Cell Dev Biol 20: 432-440.
21. Matsuyama S, Matsumoto A, Enomoto T, Nishizaki T, (2000) Activation of nicotinic acetylcholine receptors induces long-term potentiation in vivo in the intact mouse dentate gyrus. Eur J Neurosci 12: 3741-3747.
22. Placzek AN, Zhang TA, Dani JA, (2009) Nicotinic mechanisms influencing synaptic plasticity in the hippocampus. Acta Pharmacol Sin 30: 752-760.
23. Daulatzai MA, (2010) Early stages of pathogenesis in memory impairment during normal senescence and Alzheimer's disease. J Alzheimers Dis 20: 355-367.
24. Hernandez CM, Kayed R, Zheng H, Sweatt JD, Dineley KT, (2010) Loss of alpha7 nicotinic receptors enhances beta-amyloid oligomer accumulation, exacerbating early-stage cognitive decline and septohippocampal pathology in a mouse model of Alzheimer's disease. J Neurosci 30: 2442-2453.
25. Morgan SL, Teyler TJ, (2001) Electrical stimuli patterned after the theta-rhythm induce multiple forms of LTP. J Neurophysiol 86: 1289-1296.
26. Hagan JJ, Salamone JD, Simpson J, Iversen SD, Morris RG, (1988) Place navigation in rats is impaired by lesions of medial septum and diagonal band but not nucleus basalis magnocellularis. Behav Brain Res 27: 9-20.
27. Hepler DJ, Olton DS, Wenk GL, Coyle JT, (1985) Lesions in nucleus basalis magnocellularis and medial septal area of rats produce qualitatively similar memory impairments. J Neurosci 5: 866-873.
28. Kelsey JE, Landry BA, (1988) Medial septal lesions disrupt spatial mapping ability in rats. Behav Neurosci 102: 289-293.
29. M'Harzi M, Jarrard LE, (1992) Effects of medial and lateral septal lesions on acquisition of a place and cue radial maze task. Behav Brain Res 49: 159-165.
30. Miyamoto M, Kato J, Narumi S, Nagaoka A, (1987) Characteristics of memory impairment following lesioning of the basal forebrain and medial septal nucleus in rats. Brain Res 419: 19-31.
31. Mizumori SJ, Perez GM, Alvarado MC, Barnes CA, McNaughton BL, (1990) Reversible inactivation of the medial septum differentially affects two forms of learning in rats. Brain Res 528: 12-20.
32. 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.
33. Baxter MG, Gallagher M, (1996) Intact spatial learning in both young and aged rats following selective removal of hippocampal cholinergic input. Behav Neurosci 110: 460-467.
34. Frielingsdorf H, Thal LJ, Pizzo DP, (2006) The septohippocampal cholinergic system and spatial working memory in the Morris water maze. Behav Brain Res 168: 37-46.
35. Gibbs RB, Johnson DA, (2007) Cholinergic lesions produce task-selective effects on delayed matching to position and configural association learning related to response pattern and strategy. Neurobiol Learn Mem 88: 19-32.
36. Jonasson Z, Cahill JF, Tobey RE, Baxter MG, (2004) Sexually dimorphic effects of hippocampal cholinergic deafferentation in rats. Eur J Neurosci 20: 3041-3053.
37. Kirby BP, Rawlins JN, (2003) The role of the septo-hippocampal cholinergic projection in T-maze rewarded alternation. Behav Brain Res 143: 41-48.
38. McMahan RW, Sobel TJ, Baxter MG, (1997) Selective immunolesions of hippocampal cholinergic input fail to impair spatial working memory. Hippocampus 7: 130-136.
39. Winters BD, Dunnett SB, (2004) Selective lesioning of the cholinergic septo-hippocampal pathway does not disrupt spatial short-term memory: a comparison with the effects of fimbria-fornix lesions. Behav Neurosci 118: 546-562.
40. Fletcher BR, Baxter MG, Guzowski JF, Shapiro ML, Rapp PR, (2007) Selective cholinergic depletion of the hippocampus spares both behaviorally induced Arc transcription and spatial learning and memory. Hippocampus 17: 227-234.
41. Shen J, Barnes CA, Wenk GL, McNaughton BL, (1996) Differential effects of selective immunotoxic lesions of medial septal cholinergic cells on spatial working and reference memory. Behav Neurosci 110: 1181-1186.
42. van der Staay FJ, Bouger P, Lehmann O, Lazarus C, Cosquer B, et al. (2006) Long-term effects of immunotoxic cholinergic lesions in the septum on acquisition of the cone-field task and noncognitive measures in rats. Hippocampus 16: 1061-1079.
43. Fitz NF, Gibbs RB, Johnson DA, (2008) Selective lesion of septal cholinergic neurons in rats impairs acquisition of a delayed matching to position T-maze task by delaying the shift from a response to a place strategy. Brain Res Bull 77: 356-360.
44. Johnson DA, Zambon NJ, Gibbs RB, (2002) 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: 132-141.
45. Janis LS, Glasier MM, Fulop Z, Stein DG, (1998) Intraseptal injections of 192 IgG saporin produce deficits for strategy selection in spatial-memory tasks. Behav Brain Res 90: 23-34.
46. Berger-Sweeney J, Heckers S, Mesulam MM, Wiley RG, Lappi DA, et al. (1994) Differential effects on spatial navigation of immunotoxin-induced cholinergic lesions of the medial septal area and nucleus basalis magnocellularis. J Neurosci 14: 4507-4519.
47. Walsh TJ, Herzog CD, Gandhi C, Stackman RW, Wiley RG, (1996) Injection of IgG 192-saporin into the medial septum produces cholinergic hypofunction and dose-dependent working memory deficits. Brain Res 726: 69-79.
48. 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.
49. Huber KM, Mauk MD, Kelly PT, (1995) Distinct LTP induction mechanisms: contribution of NMDA receptors and voltage-dependent calcium channels. J Neurophysiol 73: 270-279.
50. Lauterborn JC, Rex CS, Kramar E, Chen LY, Pandyarajan V, et al. (2007) Brain-derived neurotrophic factor rescues synaptic plasticity in a mouse model of fragile X syndrome. J Neurosci 27: 10685-10694.
51. Cobb SR, Davies CH, (2005) Cholinergic modulation of hippocampal cells and circuits. J Physiol 562: 81-88.
52. Radcliffe KA, Fisher JL, Gray R, Dani JA, (1999) Nicotinic modulation of glutamate and GABA synaptic transmission of hippocampal neurons. Ann N Y Acad Sci 868: 591-610.
53. Muller D, Joly M, Lynch G, (1988) Contributions of quisqualate and NMDA receptors to the induction and expression of LTP. Science 242: 1694-1697.
54. Robinson HP, Kawai N, (1993) Single channel properties at the synaptic site. Exs 63: 250-265.
55. Tang CM, Shi QY, Katchman A, Lynch G, (1991) Modulation of the time course of fast EPSCs and glutamate channel kinetics by aniracetam. Science 254: 288-290.
56. Vaithianathan T, Manivannan K, Kleene R, Bahr BA, Dey MP, et al. (2005) Single channel recordings from synaptosomal AMPA receptors. Cell Biochem Biophys 42: 75-85.
57. Mayer ML, Westbrook GL, (1987) Permeation and block of N-methyl-D-aspartic acid receptor channels by divalent cations in mouse cultured central neurones. J Physiol 394: 501-527.
58. Pizzo DP, Waite JJ, Thal LJ, Winkler J, (1999) Intraparenchymal infusions of 192 IgG-saporin: development of a method for selective and discrete lesioning of cholinergic basal forebrain nuclei. J Neurosci Methods 91: 9-19.
59. Yoder RM, Pang KC, (2005) Involvement of GABAergic and cholinergic medial septal neurons in hippocampal theta rhythm. Hippocampus 15: 381-392.
60. Martin MM, Wallace DG, (2007) Selective hippocampal cholinergic deafferentation impairs self-movement cue use during a food hoarding task. Behav Brain Res 183: 78-86.
61. Monteiro Moreira K, Lima Ferreira T, Vecchio Fornari R, Perez Figueredo LZ, Menezes Oliveira MG, (2005) Interaction between M1-muscarinic and glutamatergic NMDA receptors on an inhibitory avoidance task. Brain Res Bull 67: 504-508.
62. Ohno M, Watanabe S, (1996) Interactive processing between glutamatergic and cholinergic systems involved in inhibitory avoidance learning of rats. Eur J Pharmacol 312: 145-147.
63. Ciamei A, Aversano M, Cestari V, Castellano C, (2001) Effects of MK-801 and nicotine combinations on memory consolidation in CD1 mice. Psychopharmacology (Berl) 154: 126-130.
64. Gould TJ, Lewis MC, (2005) Coantagonism of glutamate receptors and nicotinic acetylcholinergic receptors disrupts fear conditioning and latent inhibition of fear conditioning. Learn Mem 12: 389-398.
65. Levin ED, Bettegowda C, Weaver T, Christopher NC, (1998) Nicotine-dizocilpine interactions and working and reference memory performance of rats in the radial-arm maze. Pharmacol Biochem Behav 61: 335-340.
66. Tsukada H, Miyasato K, Nishiyama S, Fukumoto D, Kakiuchi T, et al. (2005) Nicotine normalizes increased prefrontal cortical dopamine D1 receptor binding and decreased working memory performance produced by repeated pretreatment with MK-801: a PET study in conscious monkeys. Neuropsychopharmacology 30: 2144-2153.
67. Figueredo LZ, Moreira KM, Ferreira TL, Fornari RV, Oliveira MG, (2008) Interaction between glutamatergic-NMDA and cholinergic-muscarinic systems in classical fear conditioning. Brain Res Bull 77: 71-76.
68. Jafari-Sabet M, (2006) NMDA receptor blockers prevents the facilitatory effects of post-training intra-dorsal hippocampal NMDA and physostigmine on memory retention of passive avoidance learning in rats. Behav Brain Res 169: 120-127.
69. Rezayof A, Shirazi-Zand Z, Zarrindast MR, Nayer-Nouri T, (2010) Nicotine improves ethanol-induced memory impairment: the role of dorsal hippocampal NMDA receptors. Life Sci 86: 260-266.
70. Levin ED, Sledge D, Baruah A, Addy NA, (2003) Ventral hippocampal NMDA blockade and nicotinic effects on memory function. Brain Res Bull 61: 489-495.
71. Andre JM, Leach PT, Gould TJ, (2011) Nicotine ameliorates NMDA receptor antagonist-induced deficits in contextual fear conditioning through high-affinity nicotinic acetylcholine receptors in the hippocampus. Neuropharmacology 60: 617-625.
72. Aigner TG, (1995) Pharmacology of memory: cholinergic-glutamatergic interactions. Curr Opin Neurobiol 5: 155-160.
73. Ovsepian SV, Anwyl R, Rowan MJ, (2004) Endogenous acetylcholine lowers the threshold for long-term potentiation induction in the CA1 area through muscarinic receptor activation: in vivo study. Eur J Neurosci 20: 1267-1275.
74. Blokland A, (1995) Acetylcholine: a neurotransmitter for learning and memory? Brain Res Brain Res Rev 21: 285-300.
75. Hasselmo ME, (1999) Neuromodulation: acetylcholine and memory consolidation. Trends Cogn Sci 3: 351-359.
76. Shinoe T, Matsui M, Taketo MM, Manabe T, (2005) Modulation of synaptic plasticity by physiological activation of M1 muscarinic acetylcholine receptors in the mouse hippocampus. J Neurosci 25: 11194-11200.
77. Auerbach JM, Segal M, (1996) Muscarinic receptors mediating depression and long-term potentiation in rat hippocampus. J Physiol 492 (Pt 2): 479-493.
78. Fernandez de Sevilla D, Nunez A, Borde M, Malinow R, Buno W, (2008) Cholinergic-mediated IP3-receptor activation induces long-lasting synaptic enhancement in CA1 pyramidal neurons. J Neurosci 28: 1469-1478.
79. Kuczewski N, Aztiria E, Leanza G, Domenici L, (2005) Selective cholinergic immunolesioning affects synaptic plasticity in developing visual cortex. Eur J Neurosci 21: 1807-1814.
80. Birthelmer A, Ehret A, Amtage F, Forster S, Lehmann O, et al. (2003) Neurotransmitter release and its presynaptic modulation in the rat hippocampus after selective damage to cholinergic or/and serotonergic afferents. Brain Res Bull 59: 371-381.
81. Yamazaki Y, Hamaue N, Sumikawa K, (2002) Nicotine compensates for the loss of cholinergic function to enhance long-term potentiation induction. Brain Res 946: 148-152.
82. Vaglenova J, Parameshwaran K, Suppiramaniam V, Breese CR, Pandiella N, et al. (2008) Long-lasting teratogenic effects of nicotine on cognition: gender specificity and role of AMPA receptor function. Neurobiol Learn Mem 90: 527-536.
83. Yamazaki Y, Jia Y, Niu R, Sumikawa K, (2006) Nicotine exposure in vivo induces long-lasting enhancement of NMDA receptor-mediated currents in the hippocampus. Eur J Neurosci 23: 1819-1828.
84. Pitler TA, Alger BE, (1992) Cholinergic excitation of GABAergic interneurons in the rat hippocampal slice. J Physiol 450: 127-142.
85. Jouvenceau A, Billard JM, Wiley RG, Lamour Y, Dutar P, (1994) Cholinergic denervation of the rat hippocampus by 192-IgG-saporin: electrophysiological evidence. Neuroreport 5: 1781-1784.
86. Jouvenceau A, Billard JM, Lamour Y, Dutar P, (1997) Potentiation of glutamatergic EPSPs in rat CA1 hippocampal neurons after selective cholinergic denervation by 192 IgG-saporin. Synapse 26: 292-300.
87. Hefft S, Hulo S, Bertrand D, Muller D, (1999) Synaptic transmission at nicotinic acetylcholine receptors in rat hippocampal organotypic cultures and slices. J Physiol 515 (Pt 3): 769-776.
88. Kanju PM, Parameshwaran K, Sims C, Bahr BA, Shonesy BC, et al. (2008) Ampakine CX516 ameliorates functional deficits in AMPA receptors in a hippocampal slice model of protein accumulation. Exp Neurol 214: 55-61.
89. Salter MW, Dong Y, Kalia LV, Liu XJ, Pitcher G, (2009) Regulation of NMDA Receptors by Kinases and Phosphatases. In: Van Dongen AM, editors. Biology of the NMDA Receptor Boca Raton (FL) CRC Press.
90. Lin Y, Jover-Mengual T, Wong J, Bennett MV, Zukin RS, (2006) PSD-95 and PKC converge in regulating NMDA receptor trafficking and gating. Proc Natl Acad Sci U S A 103: 19902-19907.
91. Xu F, Plummer MR, Len GW, Nakazawa T, Yamamoto T, et al. (2006) Brain-derived neurotrophic factor rapidly increases NMDA receptor channel activity through Fyn-mediated phosphorylation. Brain Res 1121: 22-34.
92. Kristensen AS, Jenkins MA, Banke TG, Schousboe A, Makino Y, et al. (2011) Mechanism of Ca2+/calmodulin-dependent kinase II regulation of AMPA receptor gating. Nat Neurosci 14: 727-735.
93. Banke TG, Bowie D, Lee H, Huganir RL, Schousboe A, et al. (2000) Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase. J Neurosci 20: 89-102.
94. Derkach V, Barria A, Soderling TR, (1999) Ca2+/calmodulin-kinase II enhances channel conductance of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate type glutamate receptors. Proc Natl Acad Sci U S A 96: 3269-3274.
95. Kamsler A, McHugh TJ, Gerber D, Huang SY, Tonegawa S, (2010) Presynaptic m1 muscarinic receptors are necessary for mGluR long-term depression in the hippocampus. Proc Natl Acad Sci U S A 107: 1618-1623.
96. Lim CS, Hwang YK, Kim D, Cho SH, Banuelos C, et al. (2011) Increased interactions between PKA and NF-kappaB signaling in the hippocampus following loss of cholinergic input. Neuroscience.
97. Givens B, Olton DS, (1995) Bidirectional modulation of scopolamine-induced working memory impairments by muscarinic activation of the medial septal area. Neurobiol Learn Mem 63: 269-276.
98. Markowska AL, Olton DS, Givens B, (1995) Cholinergic manipulations in the medial septal area: age-related effects on working memory and hippocampal electrophysiology. J Neurosci 15: 2063-2073.
99. Stewart M, Fox SE, (1990) Do septal neurons pace the hippocampal theta rhythm? Trends Neurosci 13: 163-168.
100. Paxinos G, Watson C, (1998) The Rat Brain in Stereotaxic Coordinates San Diego, CA Academic Press.
101. Johnson MW, Chotiner JK, Watson JB, (1997) Isolation and characterization of synaptoneurosomes from single rat hippocampal slices. J Neurosci Methods 77: 151-156.