Carbachol-induced long-term synaptic depression is enhanced during senescence at hippocampal CA3-CA1 synapses

Journal of Neurophysiology

Volumn 104, Issue 2, 2010, Pages 607-616

  Kumar, Ashok ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANISOMYCIN; CALCIUM CHANNEL L TYPE; CARBACHOL; MUSCARINIC M1 RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NIFEDIPINE;

AGED; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; HIPPOCAMPUS; LONG TERM DEPRESSION; MALE; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; SENESCENCE; SYNAPSE; SYNAPTIC TRANSMISSION;

2-AMINO-5-PHOSPHONOVALERATE; AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANISOMYCIN; CA1 REGION, HIPPOCAMPAL; CA3 REGION, HIPPOCAMPAL; CALCIUM CHANNEL BLOCKERS; CARBACHOL; CHOLINERGIC AGONISTS; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; LONG-TERM SYNAPTIC DEPRESSION; MALE; NIFEDIPINE; PATCH-CLAMP TECHNIQUES; PROTEIN SYNTHESIS INHIBITORS; RATS; RATS, INBRED F344; SYNAPSES;

EID: 77955930778     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00278.2010     Document Type: Article

References (118)

1. Amaral DG, Kurz J. 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, 1985. (Pubitemid 15244124)
2. Amenta F, Liu A, Giannella M, Pigini M, Tayebati SK, Zaccheo D. Age-related changes in the density of muscarinic cholinergic M1 and M2 receptor subtypes in pyramidal neurons of the rat hippocampus. Eur J Histochem 39: 107-116, 1995.
3. Anagnostaras SG, Murphy GG, Hamilton SE, Mitchell SL, Rahnama NP, Nathanson NM, Silva AJ. Selective cognitive dysfunction in acetylcholine M1 muscarinic receptor mutant mice. Nat Neurosci 6: 51-58, 2003.
4. Andrews JS, Jansen JH, Linders S, Princen A. Effects of disrupting the cholinergic system on short-term spatial memory in rats. Psychopharmacology 115: 485-494, 1994.
5. Araque A, Parpura V, Sanzgiri RP, Haydon PG. Glutamate-dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons. Eur J Neurosci 10: 2129-2142, 1998a. (Pubitemid 28327360)
6. Araque A, Sanzgiri RP, Parpura V, Haydon PG. Calcium elevation in astrocytes causes an NMDA receptor-dependent increase in the frequency of miniature synaptic currents in cultured hippocampal neurons. J Neurosci 18: 6822-6829, 1998b.
7. Auerbach JM, Segal M. A novel cholinergic induction of long-term potentiation in rat hippocampus. J Neurophysiol 72: 2034-2040, 1994. (Pubitemid 24325121)
8. Auerbach JM, Segal M. Muscarinic receptors mediating depression and long-term potentiation in rat hippocampus. J Physiol 492(Pt 2):479-493, 1996.
9. Aura J, Sirvio J, Riekkinen P Jr. Methoctramine moderately improves memory but pirenzepine disrupts performance in delayed non-matching to position test. Eur J Pharmacol 333: 129-134, 1997.
10. Barnes CA, Rao G, Foster TC, McNaughton BL. Region-specific age effects on AMPA sensitivity: electrophysiological evidence for loss of synaptic contacts in hippocampal field CA1. Hippocampus 2: 457-468, 1992.
11. Barnes CA, Rao G, Orr G. Age-related decrease in the Schaffer collateral-evoked EPSP in awake, freely behaving rats. Neural Plast 7: 167-178, 2000.
12. Bartus RT. On neurodegenerative diseases, models, and treatment strategies: lessons learned and lessons forgotten a generation following the cholinergic hypothesis. Exp Neurol 163: 495-529, 2000.
13. Bartus RT, Dean RL 3rd, Beer B, Lippa AS. The cholinergic hypothesis of geriatric memory dysfunction. Science 217: 408-414, 1982.
14. Benson DM, Blitzer RD, Landau EM. An analysis of the depolarization produced in guinea pig hippocampus by cholinergic receptor stimulation. J Physiol 404: 479-496, 1988.
15. Bianchi R, Wong RK. Carbachol-induced synchronized rhythmic bursts in CA3 neurons of guinea pig hippocampus in vitro. J Neurophysiol 72: 131-138, 1994. (Pubitemid 24233638)
16. Blaker SN, Armstrong DM, Gage FH. Cholinergic neurons within the rat hippocampus: response to fimbria-fornix transection. J Comp Neurol 272: 127-138, 1988.
17. Blitzer RD, Gil O, Landau EM. Cholinergic stimulation enhances long-term potentiation in the CA1 region of rat hippocampus. Neurosci Lett 119: 207-210, 1990.
18. Blitzer RD, Gil O, Omri G, Landau EM. Nifedipine blocks calcium-dependent cholinergic depolarization in the guinea pig hippocampus. Brain Res 542: 293-299, 1991.
19. 2+/calmodulin-dependent protein kinase II. J Neurosci 30: 1914-1924, 2010.
20. Bolshakov VY, Siegelbaum SA. Postsynaptic induction and presynaptic expression of hippocampal long-term depression. Science 264: 1148-1152, 1994.
21. Bonner TI, Buckley NJ, Young AC, Brann MR. Identification of a family of muscarinic acetylcholine receptor genes. Science 237: 527-532, 1987. (Pubitemid 17125922)
22. Brocher S, Artola A, Singer W. Agonists of cholinergic and noradrenergic receptors facilitate synergistically the induction of long-term potentiation in slices of rat visual cortex. Brain Res 573: 27-36, 1992.
23. Buckley NJ, Saffrey MJ, Hassall CJ, Burnstock G. Localization of muscarinic receptors on peptide-containing neurons of the guinea pig myenteric plexus in tissue culture. Brain Res 445: 152-156, 1988.
24. Burke SN, Barnes CA. Neural plasticity in the ageing brain. Nat Rev Neurosci 7: 30-40, 2006.
25. Burke SN, Barnes CA. Senescent synapses and hippocampal circuit dynamics. Trends Neurosci 33: 153-161, 2010.
26. Callahan MJ, Kinsora JJ, Harbaugh RE, Reeder TM, Davis RE. Continuous ICV infusion of scopolamine impairs sustained attention of rhesus monkeys. Neurobiol Aging 14: 147-151, 1993.
27. Caulfield MP. Muscarinic receptors - characterization, coupling and function. Pharmacol Ther 58: 319-379, 1993.
28. 2+ transients evoked by back-propagating action potentials in apical and basal dendrites of cortical pyramidal neurons. J Neurophysiol 99: 2833-2843, 2008.
29. 2+ channels to homosynaptic long-term depression in the CA1 region in vitro. J Neurophysiol 77: 1651-1655, 1997.
30. Collerton D. Cholinergic function and intellectual decline in Alzheimer's disease. Neuroscience 19: 1-28, 1986.
31. Decker MW. The effects of aging on hippocampal and cortical projections of the forebrain cholinergic system. Brain Res 434: 423-438, 1987.
32. Dekker AJ, Connor DJ, Thal LJ. The role of cholinergic projections from the nucleus basalis in memory. Neurosci Biobehav Rev 15: 299-317, 1991.
33. Deupree DL, Bradley J, Turner DA. Age-related alterations in potentiation in the CA1 region in F344 rats. Neurobiol Aging 14: 249-258, 1993. (Pubitemid 23161546)
34. Disterhoft JF, Matthew Oh M. Modulation of cholinergic transmission enhances excitability of hippocampal pyramidal neurons and ameliorates learning impairments in aging animals. Neurobiol Learn Mem 80: 223-233, 2003.
35. Dobrunz LE, Stevens CF. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18: 995-1008, 1997.
36. Drachman DA, Leavitt J. Human memory and the cholinergic system. A relationship to aging? Arch Neurol 30: 113-121, 1974.
37. Dudek SM, Bear MF. Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-d-aspartate receptor blockade. Proc Natl Acad Sci USA 89: 4363-4367, 1992.
38. Dudek SM, Bear MF. Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J Neurosci 13: 2910-2918, 1993.
39. Dumas TC, Foster TC. Development of metabotropic glutamate receptor-mediated synaptic inhibition. Neuroreport 8: 2919-2924, 1997.
40. Egorov AV, Gloveli T, Muller W. Muscarinic control of dendritic excitability and Ca(2+) signaling in CA1 pyramidal neurons in rat hippocampal slice. J Neurophysiol 82: 1909-1915, 1999.
41. Fibiger HC. Cholinergic mechanisms in learning, memory and dementia: a review of recent evidence. Trends Neurosci 14: 220-223, 1991.
42. Fornari RV, Moreira KM, Oliveira MG. Effects of the selective M1 muscarinic receptor antagonist dicyclomine on emotional memory. Learn Mem 7: 287-292, 2000.
43. Foster TC. Involvement of hippocampal synaptic plasticity in age-related memory decline. Brain Res Rev 30: 236-249, 1999.
44. Foster TC. Regulation of synaptic plasticity in memory and memory decline with aging. Prog Brain Res 138: 283-303, 2002.
45. Foster TC. Calcium homeostasis and modulation of synaptic plasticity in the aged brain. Aging Cell 6: 319-325, 2007.
46. Foster TC, Kumar A. Calcium dysregulation in the aging brain. Neuroscientist 8: 297-301, 2002.
47. Fraser DD, MacVicar BA. Cholinergic-dependent plateau potential in hippocampal CA1 pyramidal neurons. J Neurosci 16: 4113-4128, 1996. (Pubitemid 26192407)
48. Frotscher M, Leranth C. Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: a combined light and electron microscopic study. J Comp Neurol 239: 237-246, 1985.
49. Gallagher M, Colombo PJ. Ageing: the cholinergic hypothesis of cognitive decline. Curr Opin Neurobiol 5: 161-168, 1995.
50. Gaykema RP, Luiten PG, Nyakas C, Traber J. Cortical projection patterns of the medial septum-diagonal band complex. J Comp Neurol 293: 103-124, 1990.
51. Giocomo LM, Hasselmo ME. Neuromodulation by glutamate and acetylcholine can change circuit dynamics by regulating the relative influence of afferent input and excitatory feedback. Mol Neurobiol 36: 184-200, 2007.
52. Haas HL. Cholinergic disinhibition in hippocampal slices of the rat. Brain Res 233: 200-204, 1982. (Pubitemid 12213673)
53. Hagan JJ, Jansen JH, Broekkamp CL. Blockade of spatial learning by the M1 muscarinic antagonist pirenzepine. Psychopharmacology 93: 470-476, 1987.
54. Halliwell JV, Adams PR. Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain Res 250: 71-92, 1982.
55. Hasselmo ME. Neuromodulation: acetylcholine and memory consolidation. Trends Cogn Sci 3: 351-359, 1999.
56. Huber KM, Kayser MS, Bear MF. Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288: 1254-1257, 2000.
57. Huerta PT, Lisman JE. Heightened synaptic plasticity of hippocampal CA1 neurons during a cholinergically induced rhythmic state. Nature 364: 723-725, 1993.
58. Hunter AJ, Roberts FF. The effect of pirenzepine on spatial learning in the Morris Water Maze. Pharmacol Biochem Behav 30: 519-523, 1988.
59. 2+ mobilization in cultured rat hippocampal neurones. J Physiol 511: 747-759, 1998.
60. Ito T, Miura Y, Kadokawa T. Physostigmine induces in rats a phenomenon resembling long-term potentiation. Eur J Pharmacol 156: 351-359, 1988.
61. Jiang F, Khanna S. Microinjection of carbachol in the supramammillary region suppresses CA1 pyramidal cell synaptic excitability. Hippocampus 16: 891-905, 2006.
62. Jouvenceau A, Dutar P, Billard JM. Alteration of NMDA receptor-mediated synaptic responses in CA1 area of the aged rat hippocampus: contribution of GABAergic and cholinergic deficits. Hippocampus 8: 627-637, 1998.
63. Kamsler A, McHugh TJ, Gerber D, Huang SY, Tonegawa S. Presynaptic m1 muscarinic receptors are necessary for mGluR long-term depression in the hippocampus. Proc Natl Acad Sci USA 107: 1618-1623, 2010.
64. Kang J, Jiang L, Goldman SA, Nedergaard M. Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat Neurosci 1: 683-692, 1998. (Pubitemid 128406379)
65. Kasa P, Rakonczay Z, Gulya K. The cholinergic system in Alzheimer's disease. Prog Neurobiol 52: 511-535, 1997.
66. Kemp N, McQueen J, Faulkes S, Bashir ZI. Different forms of LTD in the CA1 region of the hippocampus: role of age and stimulus protocol. Eur J Neurosci 12: 360-366, 2000.
67. Kimura F. Cholinergic modulation of cortical function: a hypothetical role in shifting the dynamics in cortical network. Neurosci Res 38: 19-26, 2000.
68. Kimura F, Baughman RW. Distinct muscarinic receptor subtypes suppress excitatory and inhibitory synaptic responses in cortical neurons. J Neurophysiol 77: 709-716, 1997.
69. Kirkwood A, Rozas C, Kirkwood J, Perez F, Bear MF. Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine. J Neurosci 19: 1599-1609, 1999.
70. Kojima J, Onodera K. NIK-247 induces long-term potentiation of synaptic transmission in the CA1 region of rat hippocampal slices through M2 muscarinic receptors. Gen Pharmacol 31: 297-300, 1998. (Pubitemid 28288407)
71. Kremin T, Gerber D, Giocomo LM, Huang SY, Tonegawa S, Hasselmo ME. Muscarinic suppression in stratum radiatum of CA1 shows dependence on presynaptic M1 receptors and is not dependent on effects at GABA(B) receptors. Neurobiol Learn Mem 85: 153-163, 2006.
72. Kumar A, Foster TC. Enhanced long-term potentiation during aging is masked by processes involving intracellular calcium stores. J Neurophysiol 91: 2437-2444, 2004. (Pubitemid 38649754)
73. Kumar A, Foster TC. Shift in induction mechanisms underlies an age-dependent increase in DHPG-induced synaptic depression at CA3 CA1 synapses. J Neurophysiol 98: 2729-2736, 2007.
74. Kumar A, Thinschmidt JS, Foster TC, King MA. Aging effects on the limits and stability of long-term synaptic potentiation and depression in rat hippocampal area CA1. J Neurophysiol 98: 594-601, 2007.
75. 2+ ratios on frequency potentiation in hippocampal slices of young and aged rats. J Neurophysiol 56: 797-811, 1986.
76. Lewis PR, Shute CC, Silver A. Confirmation from choline acetylase analyses of a massive cholinergic innervation to the rat hippocampus. J Physiol 191: 215-224, 1967.
77. Li S, Cullen WK, Anwyl R, Rowan MJ. Muscarinic acetylcholine receptor-dependent induction of persistent synaptic enhancement in rat hippocampus in vivo. Neuroscience 144: 754-761, 2007. (Pubitemid 44855314)
78. Luscher C, Huber KM. Group 1 mGluR-dependent synaptic long-term depression: mechanisms and implications for circuitry and disease. Neuron 65: 445-459, 2010.
79. Markram H, Segal M. Long-lasting facilitation of excitatory postsynaptic potentials in the rat hippocampus by acetylcholine. J Physiol 427: 381-393, 1990.
80. Massey PV, Bhabra G, Cho K, Brown MW, Bashir ZI. Activation of muscarinic receptors induces protein synthesis-dependent long-lasting depression in the perirhinal cortex. Eur J Neurosci 14: 145-152, 2001.
81. McCoy PA, McMahon LL. Muscarinic receptor dependent long-term depression in rat visual cortex is PKC independent but requires ERK1/2 activation and protein synthesis. J Neurophysiol 98: 1862-1870, 2007.
82. McCoy P, Norton TT, McMahon LL. Layer 2/3 synapses in monocular and binocular regions of tree shrew visual cortex express mAChR-dependent long-term depression and long-term potentiation. J Neurophysiol 100: 336-345, 2008.
83. McCutchen E, Scheiderer CL, Dobrunz LE, McMahon LL. Coexistence of muscarinic long-term depression with electrically induced long-term potentiation and depression at CA3-CA1 synapses. J Neurophysiol 96: 3114-3121, 2006.
84. McKinney M, Jacksonville MC. Brain cholinergic vulnerability: relevance to behavior and disease. Biochem Pharmacol 70: 1115-1124, 2005. (Pubitemid 41317506)
85. Messer WS, Jr, Bohnett M, Stibbe J. Evidence for a preferential involvement of M1 muscarinic receptors in representational memory. Neurosci Lett 116: 184-189, 1990.
86. Mesulam M. The cholinergic lesion of Alzheimer's disease: pivotal factor or side show? Learn Mem 11: 43-49, 2004.
87. Mrzljak L, Levey AI, Goldman-Rakic PS. Association of m1 and m2 muscarinic receptor proteins with asymmetric synapses in the primate cerebral cortex: morphological evidence for cholinergic modulation of excitatory neurotransmission. Proc Natl Acad Sci USA 90: 5194-5198, 1993.
88. Mulkey RM, Malenka RC. Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 9: 967-975, 1992.
89. Muller W, Misgeld U. Slow cholinergic excitation of guinea pig hippocampal neurons is mediated by two muscarinic receptor subtypes. Neurosci Lett 67: 107-112, 1986. (Pubitemid 16034531)
90. Nicoll RA, Malenka RC, Kauer JA. Functional comparison of neurotransmitter receptor subtypes in mammalian central nervous system. Physiol Rev 70: 513-565, 1990.
91. 2+ channels. J Neurosci 18: 3171-3179, 1998.
92. Norris CM, Korol DL, Foster TC. Increased susceptibility to induction of long-term depression and long- term potentiation reversal during aging. J Neurosci 16: 5382-5392, 1996.
93. Nosyreva ED, Huber KM. Developmental switch in synaptic mechanisms of hippocampal metabotropic glutamate receptor-dependent long-term depression. J Neurosci 25: 2992-3001, 2005.
94. Oh MM, Power JM, Thompson LT, Moriearty PL, Disterhoft JF. Metrifonate increases neuronal excitability in CA1 pyramidal neurons from both young and aging rabbit hippocampus. J Neurosci 19: 1814-1823, 1999.
95. Oliet SH, Malenka RC, Nicoll RA. Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neuron 18: 969-982, 1997.
96. Parpura V, Basarsky TA, Liu F, Jeftinija K, Jeftinija S, Haydon PG. Glutamate-mediated astrocyte-neuron signalling. Nature 369: 744-747, 1994.
97. Patil MM, Linster C, Lubenov E, Hasselmo ME. Cholinergic agonist carbachol enables associative long-term potentiation in piriform cortex slices. J Neurophysiol 80: 2467-2474, 1998.
98. Pitler TA, Alger BE. Cholinergic excitation of GABAergic interneurons in the rat hippocampal slice. J Physiol 450: 127-142, 1992.
99. Rosenzweig ES, Barnes CA. Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog Neurobiol 69: 143-179, 2003.
100. Rouse ST, Marino MJ, Potter LT, Conn PJ, Levey AI. Muscarinic receptor subtypes involved in hippocampal circuits. Life Sci 64: 501-509, 1999.
101. Sajikumar S, Frey JU. Anisomycin inhibits the late maintenance of long-term depression in rat hippocampal slices in vitro. Neurosci Lett 338: 147-150, 2003.
102. Sala M, Braida D, Calcaterra P, Leone MP, Comotti FA, Gianola S, Gori E. Effect of centrally administered atropine and pirenzepine on radial arm maze performance in the rat. Eur J Pharmacol 194: 45-49, 1991.
103. Sanchez G, Alvares Lde O, Oberholzer MV, Genro B, Quillfeldt J, da Costa JC, Cervenansky C, Jerusalinsky D, Kornisiuk E. M4 muscarinic receptors are involved in modulation of neurotransmission at synapses of Schaffer collaterals on CA1 hippocampal neurons in rats. J Neurosci Res 87: 691-700, 2009.
104. Scheiderer CL, McCutchen E, Thacker EE, Kolasa K, Ward MK, Parsons D, Harrell LE, Dobrunz LE, McMahon LL. Sympathetic sprouting drives hippocampal cholinergic reinnervation that prevents loss of a muscarinic receptor-dependent long-term depression at CA3-CA1 synapses. J Neurosci 26: 3745-3756, 2006.
105. Scheiderer CL, Smith CC, McCutchen E, McCoy PA, Thacker EE, Kolasa K, Dobrunz LE, McMahon LL. Coactivation of M(1) muscarinic and alpha1 adrenergic receptors stimulates extracellular signal-regulated protein kinase and induces long-term depression at CA3-CA1 synapses in rat hippocampus. J Neurosci 28: 5350-5358, 2008.
106. Schliebs R. Basal forebrain cholinergic dysfunction in Alzheimer's disease-interrelationship with beta-amyloid, inflammation and neurotrophin signaling. Neurochem Res 30: 895-908, 2005. (Pubitemid 41413946)
107. 2+-elevating muscarinic cholinergic and histaminergic receptors in situ. J Neurochem 74: 555-563, 2000.
108. Shimoshige Y, Maeda T, Kaneko S, Akaike A, Satoh M. Involvement of M2 receptor in an enhancement of long-term potentiation by carbachol in Schaffer collateral-CA1 synapses of hippocampal slices. Neurosci Res 27: 175-180, 1997.
109. Shinoe T, Matsui M, Taketo MM, Manabe T. Modulation of synaptic plasticity by physiological activation of M1 muscarinic acetylcholine receptors in the mouse hippocampus. J Neurosci 25: 11194-11200, 2005.
110. Shirey JK, Xiang Z, Orton D, Brady AE, Johnson KA, Williams R, Ayala JE, Rodriguez AL, Wess J, Weaver D, Niswender CM, Conn PJ. An allosteric potentiator of M4 mAChR modulates hippocampal synaptic transmission. Nat Chem Biol 4: 42-50, 2008.
111. Strong R, Hicks P, Hsu L, Bartus RT, Enna SJ. Age-related alterations in the rodent brain cholinergic system and behavior. Neurobiol Aging 1: 59-63, 1980.
112. Tayebati SK, Amenta F, El-Assouad D, Zaccheo D. Muscarinic cholinergic receptor subtypes in the hippocampus of aged rats. Mech Ageing Dev 123: 521-528, 2002. (Pubitemid 34127681)
113. Thiels E, Barrionuevo G, Berger TW. Excitatory stimulation during postsynaptic inhibition induces long-term depression in hippocampus in vivo. J Neurophysiol 72: 3009-3016, 1994.
114. Valentino RJ, Dingledine R. Presynaptic inhibitory effect of acetylcholine in the hippocampus. J Neurosci 1: 784-792, 1981.
115. Vilaro MT, Mengod G, Palacios G, Palacios JM. Receptor distribution in the human and animal hippocampus: focus on muscarinic acetylcholine receptors. Hippocampus 3 Spec No: 149-156, 1993.
116. Volk LJ, Pfeiffer BE, Gibson JR, Huber KM. Multiple Gq-coupled receptors converge on a common protein synthesis-dependent long-term depression that is affected in fragile X syndrome mental retardation. J Neurosci 27: 11624-11634, 2007.
117. Williams S, Johnston D. Muscarinic depression of long-term potentiation in CA3 hippocampal neurons. Science 242: 84-87, 1988.
118. Wu WW, Chan CS, Disterhoft JF. Slow afterhyperpolarization governs the development of NMDA receptor-dependent afterdepolarization in CA1 pyramidal neurons during synaptic stimulation. J Neurophysiol 92: 2346-2356, 2004.