毒蕈碱型胆碱能系统对海马突触传递和可塑性的调控及铅的作用
|
摘要
胆碱能系统可以影响海马突触传递和突触可塑性,从而在海马的学习和记忆功能扮演着重要的角色。胆碱能调控作用主要通过毒蕈碱型胆碱受体(mAChR)。毒蕈碱型胆碱受体有M_1-M_5五种亚型,关于这五种亚型在胆碱的突触传递和突触可塑性调控中所起到的作用,目前仍不是十分清楚。铅是环境中的一种重金属污染物,具有神经毒性。铅暴露对多种递质系统以及神经系统功能都造成损伤。对于胆碱能调控是否也包括在铅的神经毒理内很少见报道。本文运用电生理学实验方法,研究海马中毒蕈碱型胆碱能系统对突触传递和突触可塑性的调控以及铅对这种胆碱能调控的影响。
1.在海马齿状回区域(DG)内注射各种毒蕈碱型胆碱受体配体,在位记录兴奋性突触后电位,研究各种毒蕈碱型胆碱受体在突触传递和可塑性调控中的作用。结果表明,一种非选择性毒蕈碱型胆碱受体阻断剂阿托品可以压抑长时程增强(LTP)的诱导,证实了海马内毒蕈碱型胆碱系统参与了LTP的诱导。我们研究了M_(2/4)型胆碱受体拮抗剂和M_(3/5)AChR型胆碱受体拮抗剂对LTP的影响。发现向海马内注射M_1型胆碱受体拈抗剂和M_(2/4)型胆碱受体拮抗剂可以明显压抑LIP的诱导,而M_(3/5)AChR型胆碱受体拮抗剂则对LTP没有作用。结果表明毒蕈碱型胆碱能系统对突触传递和突触可塑性的调控是通过不同的受体亚型实现的。
2.应用离体记录技术,研究了大鼠海马雪氏侧枝—CA1锥体神经元突触传递的毒蕈碱型胆碱能调控及铅对这种调控的作用。carbachol是胆碱能受体的激动剂。在本实验中,灌流5 M carbacbol使大鼠海马CA1锥体神经元的谷氨酸能EPSC幅度减小,这种抑制效应主要是由M型乙酰胆碱受体介导的。在使用美加明(mecamylamine,10M)阻断N型乙酰胆碱受体的作用后,carbacbol通过M型胆碱受体介导浓度依赖性地抑制EPSC;5M carbacbol增强了双脉冲易化效应和10Hz串刺激反应;并且降低了sEPSCs的频率,减小了sEPSCs的幅度和衰减时间。在相同条件下,10M铅离子灌流对于谷氨酸能EPSC的幅度没有显著性的影响,但是轻微地削弱了carbacbol对EPSC的压抑作用;铅抑制了carbachol对PPF和串刺激反应的增强作用;10 M铅降低了sEPSCs的频率和衰减,并且阻断了carbachol的进一步作用;10 M铅对sEPSCs的幅度没有显著性的作用,而且对carbachol的抑制作用也没有显著影响。胆碱能系统通过突触前和突触后的mAChRs对海马的突触传递和突触可塑性的调控作用,对学习和记忆功能有重要的意义。铅可能通过损伤谷氨酸能突触传递的胆碱能调控作用来影响突触传递效能和突触可塑性,可能是铅损伤学习记忆功能的机制之一。
The roles of the muscarinic acetylcholine receptors(mAChRs)in synaptic transmission and Plasticity at many areas of the central nervous system including the hippocampus,have been extensively studied.However,not much is known about the modulation of LTP through individual subtypes of mAChR(M1-M5 subtype).Lead, known as a heavy metal pollutant,is a neurotoxicant.Lead exposure impairs many neurotransmitter systems and nerve system function.Few has been reported about whether lead can affect muscarinic modulation.In this study,using electrophysiological methods,we investigated muscarinic modulation on synaptic transmission and Plasticity and the effect of lead on it.
1)we investigated the involvement of each individual subtypes of mAChR in LTP induction by intrahippocampal administration of cholinergic ligands at the dentate gyrus(DG)of anaesthetized rats.We found atropine,an antagonist of mAChRs,suppressed the induction of LTP.This observation confirmed that the muscarinic system is involved in LTP.We then examined the effects of M1AChR antagonists(pirenzepine and telenzepine),M2/4AChR antagonists(Methoctramine and{11-[[2-[(diethylamino)methyl]-1-piperidinyl]acetyl]-5,11 -dihydro-6H-pyrido[2, 3-b][1,4]benzodiazepin-6-one}(AFDX-116)),and M3/5AChR antagonist (4-diphenylacetoxy-N-methylpiperidine methiodide(4-DAMP))on LTP.Our results showed that both M1AChR and M2/4AChR antagonists but not M3/5AChR antagonist suppressed the amplitude of LTP.We also examined the effects of these cholinergic ligands on basal synaptic transmission and found that only pirenzepine augmented the amplitude of population spike(PS).This study suggests that individual mAChR subtypes play different modulation roles in LTP induction in the DG of rats.
2)we investigated the the muscarinic modulation in the CA1 area of hippocampal slices and the effect of lead on it.Carbachol is an agonist of cholinergic receptors.In this study,application of 5 M carbacbol by perfusion inhibited the amplitude of glutamatergic EPSC in rat hippocampal CA1 pyramidal neurons.This inhibition was maily mediated by mAChRs.With the nAChRs blocked by perfusion of mecamylamine(10 M),carbachol inhibited EPSC concentration-dependently;
5 M carbachol enhanced paired-pulse facilitation(PPF)and responses to 10 Hz train of pulses;5 M carbachol also reduced sEPSCs frequency and decreased the amplitudes and decay time of sEPSCs.In the same conditions,10 M lead showed no slgnificant effect on the amplitude of EPSC,but slightly weakened the inhibition of carbachol on EPSC;lead inhibited the enhancement of PPF and responses to 10 Hz train of pulses;and lead reduced the frequency and decay of sEPSCs,and blocked the effect of carbachol while did not has significant effect on sEPSCs amplitudes and the inhibition by carbachol.Cholinergic system modulates synaptic transmission and plasticity in hippocampus through pre- and postsynaptic mAChRs, and plays an important role in learning and memory.The effects of lead on the cholinergic modulation of glutamatergic synaptic transmission and plasticity might be involved in the impairment of learning and memory by lead.
1.在海马齿状回区域(DG)内注射各种毒蕈碱型胆碱受体配体,在位记录兴奋性突触后电位,研究各种毒蕈碱型胆碱受体在突触传递和可塑性调控中的作用。结果表明,一种非选择性毒蕈碱型胆碱受体阻断剂阿托品可以压抑长时程增强(LTP)的诱导,证实了海马内毒蕈碱型胆碱系统参与了LTP的诱导。我们研究了M_(2/4)型胆碱受体拮抗剂和M_(3/5)AChR型胆碱受体拮抗剂对LTP的影响。发现向海马内注射M_1型胆碱受体拈抗剂和M_(2/4)型胆碱受体拮抗剂可以明显压抑LIP的诱导,而M_(3/5)AChR型胆碱受体拮抗剂则对LTP没有作用。结果表明毒蕈碱型胆碱能系统对突触传递和突触可塑性的调控是通过不同的受体亚型实现的。
2.应用离体记录技术,研究了大鼠海马雪氏侧枝—CA1锥体神经元突触传递的毒蕈碱型胆碱能调控及铅对这种调控的作用。carbachol是胆碱能受体的激动剂。在本实验中,灌流5 M carbacbol使大鼠海马CA1锥体神经元的谷氨酸能EPSC幅度减小,这种抑制效应主要是由M型乙酰胆碱受体介导的。在使用美加明(mecamylamine,10M)阻断N型乙酰胆碱受体的作用后,carbacbol通过M型胆碱受体介导浓度依赖性地抑制EPSC;5M carbacbol增强了双脉冲易化效应和10Hz串刺激反应;并且降低了sEPSCs的频率,减小了sEPSCs的幅度和衰减时间。在相同条件下,10M铅离子灌流对于谷氨酸能EPSC的幅度没有显著性的影响,但是轻微地削弱了carbacbol对EPSC的压抑作用;铅抑制了carbachol对PPF和串刺激反应的增强作用;10 M铅降低了sEPSCs的频率和衰减,并且阻断了carbachol的进一步作用;10 M铅对sEPSCs的幅度没有显著性的作用,而且对carbachol的抑制作用也没有显著影响。胆碱能系统通过突触前和突触后的mAChRs对海马的突触传递和突触可塑性的调控作用,对学习和记忆功能有重要的意义。铅可能通过损伤谷氨酸能突触传递的胆碱能调控作用来影响突触传递效能和突触可塑性,可能是铅损伤学习记忆功能的机制之一。
The roles of the muscarinic acetylcholine receptors(mAChRs)in synaptic transmission and Plasticity at many areas of the central nervous system including the hippocampus,have been extensively studied.However,not much is known about the modulation of LTP through individual subtypes of mAChR(M1-M5 subtype).Lead, known as a heavy metal pollutant,is a neurotoxicant.Lead exposure impairs many neurotransmitter systems and nerve system function.Few has been reported about whether lead can affect muscarinic modulation.In this study,using electrophysiological methods,we investigated muscarinic modulation on synaptic transmission and Plasticity and the effect of lead on it.
1)we investigated the involvement of each individual subtypes of mAChR in LTP induction by intrahippocampal administration of cholinergic ligands at the dentate gyrus(DG)of anaesthetized rats.We found atropine,an antagonist of mAChRs,suppressed the induction of LTP.This observation confirmed that the muscarinic system is involved in LTP.We then examined the effects of M1AChR antagonists(pirenzepine and telenzepine),M2/4AChR antagonists(Methoctramine and{11-[[2-[(diethylamino)methyl]-1-piperidinyl]acetyl]-5,11 -dihydro-6H-pyrido[2, 3-b][1,4]benzodiazepin-6-one}(AFDX-116)),and M3/5AChR antagonist (4-diphenylacetoxy-N-methylpiperidine methiodide(4-DAMP))on LTP.Our results showed that both M1AChR and M2/4AChR antagonists but not M3/5AChR antagonist suppressed the amplitude of LTP.We also examined the effects of these cholinergic ligands on basal synaptic transmission and found that only pirenzepine augmented the amplitude of population spike(PS).This study suggests that individual mAChR subtypes play different modulation roles in LTP induction in the DG of rats.
2)we investigated the the muscarinic modulation in the CA1 area of hippocampal slices and the effect of lead on it.Carbachol is an agonist of cholinergic receptors.In this study,application of 5 M carbacbol by perfusion inhibited the amplitude of glutamatergic EPSC in rat hippocampal CA1 pyramidal neurons.This inhibition was maily mediated by mAChRs.With the nAChRs blocked by perfusion of mecamylamine(10 M),carbachol inhibited EPSC concentration-dependently;
5 M carbachol enhanced paired-pulse facilitation(PPF)and responses to 10 Hz train of pulses;5 M carbachol also reduced sEPSCs frequency and decreased the amplitudes and decay time of sEPSCs.In the same conditions,10 M lead showed no slgnificant effect on the amplitude of EPSC,but slightly weakened the inhibition of carbachol on EPSC;lead inhibited the enhancement of PPF and responses to 10 Hz train of pulses;and lead reduced the frequency and decay of sEPSCs,and blocked the effect of carbachol while did not has significant effect on sEPSCs amplitudes and the inhibition by carbachol.Cholinergic system modulates synaptic transmission and plasticity in hippocampus through pre- and postsynaptic mAChRs, and plays an important role in learning and memory.The effects of lead on the cholinergic modulation of glutamatergic synaptic transmission and plasticity might be involved in the impairment of learning and memory by lead.
引文
Abe T, Sugihara H, Shigemoto R et al. Molecular characterization of a novel metabotropic glutamate receptor mGluR5 coupled to inositol phosphate/Ca~(2+) signal transduction. J Biol Chem (1992)267: 13361-13368.
Abeliovich A, Coan C, Goda Y et al. Modified hippocampal long-term potentiation in γ-PKC mutant mice. Cell (1993) 75:1253-1262.
Alford S, Frengurli BG, Schofield JG et al. Characterization of Ca~(2+) signals induced in hippocampal CA1 neurons by synaptic activation of NMDA receptors. J Physiol (London) (1993)469: 693-716.
Bashir ZI, Jane DE, Sunter DC et al. Metabotropic glutamate receptors contribute to the induction of long-term depression in the CA1 region of the hippocampus. Eur J Pharmacol (1993)239: 265-266.
Bear MF, Dudek SM and Gold JT. Homosynaptic long-term depression in CA1 of rat hippocampus in vitro. Soc Neurosci Abstr (1992) 17: 533P.
Berger TW. Long-term potentiation of hippocampal synaptic transmission affects rate of behavioral learning. Science (1984) 224: 627-630.
Bliss TV. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol (1973) 232:331-356.
Bliss TV and Collibgridge GL. A synaptic model of memory: long-term potentiation in the hippocampus. Nature (1993) 361: 31-39.
Bolshakov VY and Siegelbaum SA. Postsynaptic induction and pre-synaptic expression of hippocampal long-term depression. Science (1994) 264: 1148-1152.
Christie BR, Kerr DS and Abraham WC. The flip side of synaptic plasticity: long-term depression mechanisms in the hippocampus. Hippocampus (1994) 4: 127-135.
Cummings JA, Nicolas SM and Malenka RC. Induction in the rat hippocampus of long-term potentiation(LTP) and long-term depression(LTD) in the presence of nitric oxide synthase inhibitor. Neurosci Lett (1994) 176: 110-114.
Duvoisin RM, Zhang C and Ramonell K. A novel metabotropic glutamate receptor expressed in the retina and olfatory bulb. J Neurosci (1995) 15: 3075-3083.
Dudek SM and Bear MF. Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J Neurosci (1993) 13: 2910-2918.
Dunwiddie T and Lynch G Long-term potentiation and depression of synaptic responses in the rat hippocampus: location, frequency dependency. J Physiol (London) (1978) 276: 353-367.
Fleischer S and Inui M. Biochemistry and biophysics of excitation- contraction coupling. Ann Rev Biophys Biophys Chem (1989) 18: 333-364.
Galione A, White A, Willmot N et al. cGMP mobilizes intracellular Ca2+ in sea urchin eggs by stimulating cyclic ADP-ribose synthesis. Nature (1993) 365: 456-459.
Griffith WH. Voltage-clamp analysis of posttetanic potentiation of mossy fiber to CA3 synapse in hippocampus. J Neurophysiol (1990) 63: 491-501.
Hebb DO. The organization of behavior. Wiley, New York (1949).
Izumi Y and Zorumski CF. Nitric oxide and long-term synaptic depression in the rat hippocampus. Neuroreport (1993) 4: 1131-1134.
Kirkwood A, Aizenman CD and Bear MF. Common forms of plasticity in hippocampus and visual cortex in vitro. Soc Neurosci Abstr (1994) 18: 1499.
Kirkwood A and Bear MF. Homosynaptic long-term depression in the visual cortex. J Neurosci (1994) 14: 3404-3412.
Kobayashi K, Manabe T and Takahashi T. Presynaptic long-term depression at the hippocampal mossy fiber-CA3 synapse. Science 273: 648—650.
Linden DJ and Connor JA. Long-term depression. Ann Rev Neurosci (1995) 18: 319-357.
Lisman J. A mechanism for the Hebb and the anti-Hebb process underlying learning and memory.Proc Natl Acad Sci USA (1989) 86: 9574-9578.
Phelps ME. An investigation of a double-tracer technique for positron computerized tomography.J Nucl Med(1982)23: 816-822.
Malenka RC, Lancaster B and Zucker RS. Temporal limits on the rise in postsynaptic calcium required for the induction of long-term potentiation. Neuron (1993) 9: 121-128.
Manahan-Vaughan D. Group 1 and 2 metabotropic glutamate receptor play differential roles in hippocampal long-term depression and long-term potentiation in freely moving rats. J Neurosci (1997) 17(9): 3303-3311.
Masu M. Tanabe Y. Tsuchida K et al. Sequence and expression of a metabotropic glutamate receptor. Nature (1991) 349: 760-765.
McPherson PS and Kim YK. The brain ryanodine receptor: a caffeine- sensitive calcium release channel. Neuron (1991) 7: 17-75.
Meszaros LG. Bak J and Chu A. Cyclic ADP-ribose as an endogenous regulator of the non-skeletal type ryanodine receptor Ca2+ channel. Nature (1993) 364: 76-79.
Miyakawa H, Ross WN, Jaffe DB et al. Synaptically activated increases in Ca2+ concentration in hippocampal pyramidal cells are primarily due to voltage-gated Ca2+ channels. Neuron (1992) 9: 1163-1173.
Monaghan D. Distribution of NMD A-sensitive L-[3H] glutamate-binding sites in rat brain. J Neurosci(1987) 329: 724-726.
Mulkey RM and Malenka RC. Mechanisms underlying inductionof homosynaptic long-term depression in area CA1 of the hippocampus. Neuron (1992) 9: 967-975.
Muller W and Connor JA. Synaptic Ca2+ responses in dendritic spines: the spine as an individual neuronal compartment. Nature (1991) 354: 73-76.
Mulkey RM. Herron CE and Malenka RC. An essential role for protein phosphatases in hippocampal long-term depression. Science (1993) 261: 1051-1055.
Nakajima Y. Iwakabe H, Akazawa C et al. Molecular of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-amino-4-phosphonobutyrate. J Biol Chem (1993) 268: 11868-11873.
O'Dell TJ and Kandel ER. Low-frequency stimulation erases LTP through an NMDA receptor-mediated activation of protein phosphatases. Leam Mem (1994) 1: 129-139.
Okamoto Ni Horis S. Akazawa C et al. Molecular characterization of a novel metabotropic glutamate receptor mGluR7 coupled to inhibitory cyclic AMP signal transduction. J Biol Chem (1994) 269: 1231-1236.
O'Mara SM, Rowan MJ and Anwyl R. Dantrolene inhibits long-term depression and depotentiation of synaptic transmission in the rat dentate gyrus. Neuroscience (1995) 68:621-624.
O'Mara SM, Rowan MJ and Anwyl R. Metabotropic glutamate receptor-induced long-term depression and depotentiation in the dentate gyrus of the rat hippocampus in vitro.Neuropharmacology(1995)34: 983-989.
Perkel DJ, Petrozzino JJ. Nicoll RA et al. The role of Ca2+ entry via synaptically activated NMDA receptors in the induction of long-term potentiation. Neuron (1993) 11: 817-823.
Pozzo-Miller LD, Petrozzino JJ, Mahanty NK et al. Optical imaging of cytosolic calcium,electrophysiology, and ultrastructure in pyramidal neurons of organotypic slice cultures from rat hippocampus. Neuroimage (1993) 1: 109-20
Racine RJ. Milgram NW and Hafner S. Long-term potentiation phenomena in the rat limbic forebrain. Brain Res (1983) 260: 217-232.
Regehr WG. Connor JA and Tank DW. Optical imaging of calcium accumulation in hippocampal pyramidal cells during synaptic activation. Nature (1989) 341: 533-536.
Regehr WG and Tank DW. Calcium concentration dynamics produced by synaptic activation of CA1 hippocampal pyramidal cells. J Neurosci (1992) 12: 4202-4223.
Reyes M and Stanton PK.Induction of hippocampal long-term depression required release of Ca2+ from separate presynaptic and postsynaptic intracellular stores.J Neurosci(1996)16(19):5951-5960.
Robinson GB and Racine RJ.Heterosynaptic interactions between septal and entorhinai inputs to the dentate gyrus:long-term potentiation effects.Brain Res(1982)249:162-166.
Schuman FM,Meffert MK,Schulman H et al.An ADP-ribosyltransferase as a potential target for nitric oxide action in hippocampal long-term potentiation.Proc Natl Acad Sci USA(1994)91:11958-11962.
Scoville WB and Milner B.Loss of recent memory after bilateral hippocampal lesions.J Neurol Neurosurg Psych(1957)20:11-21.
Selig DK,Lee HK,Bear MF et al.Reexamination of the effects of MCPG on hippocampal LTP,LTD,and depotentiation.J Neurophysiol(1995)74:1075-1082.
Stevens CF and Wang Y.Reversal of long-term potentiation by inhibitor of haem oxygenase.Nature(1993)364:147-149.
Tanabe Y,Masu M,Ishii T et al.A family of metabotropic glutamate receptors.Neuron(1992)8:169-179.
Tanabe Y,Normura A,Masu M et al.Signal transduction,pharmacological properties,and expression patterns of two rat metabotropic glutamate receptors,mGluR3 and mGluR4.J Neurosci(1993)13:1372-1378.
Tsumoto T.Long-term depression in cerebral cortex:a possible substrate of "forgetting" that should not be forgotten.Neurosci Res(1993)16:263-270.
Vincent SR.Neurons that say NO.TINS(1992)15:108-113.
Wang Y,Rowan MJ and Anwyl R.Induction of LTD in the dentate gyrus in vitro is NMDA receptor independent but dependent on Ca2+ influx via low-voltage-activated Ca2+ channel and release of Ca2+ from intracellular stores.J Neurophysiology(1997)77:812-825.
Yokoi M,Kobayashi K,Manabe T et al.Impairment of hippocampal mossy fiber LTD in mice lacking mGluR2.Science(1996)273:645P.
Zorumski CF and Izumi Y,Nitric oxide and hippocampal synaptic plasticity.BioChem Pharmacol(1993)46:477-485.
韩太真,关于长时程增强形成机制的研究进展.生理科学进展.(1994)25:60-63
韩太真、吴馥梅主编,学习与记忆的神经生物学 北京医科大学、中国协和大学联合出版社,(1998).
Alkondon, M., Pereira, E. F., Barbosa, C. T. and Albuquerque, E. X., 1997. Neuronal nicotinic acetylcholine receptor activation modulates gamma-aminobutyric acid release from CA1 neurons of rat hippocampal slices. J Pharmacol Exp Then 283,1396-1411.
Altmann, L., Weinsberg, F., Sveinsson, K., Lilienthal, H., Wiegand, H. and Winneke, G, 1993.Impairment of long-term potentiation and learning following chronic lead exposure.Toxicol Lett. 66, 105-112.
Auerbach, J. M. and Segal, M., 1994. A novel cholinergic induction of long-term potentiation in rat hippocampus. J Neurophysiol. 72,2034-2040.
Bartus, R. T., Dean, R. L., 3rd, Beer, B. and Lippa, A. S., 1982. The cholinergic hypothesis of geriatric memory dysfunction. Science. 217,408-414.
Benardo, L. S. and Prince, D. A., 1982. Cholinergic excitation of mammalian hippocampal pyramidal cells. Brain Res. 249,315-331.
Bielarczyk, H., Tomsig, J. L. and Suszkiw, J. B., 1994. Perinatal low-level lead exposure and the septo-hippocampal cholinergic system: selective reduction of muscarinic receptors and cholineacetyltransferase in the rat septum. Brain Res. 643, 211 -217.
Bland, B. H., Colom, L. V., Konopacki, J. and Roth, S. H., 1988. Intracellular records of carbachol-induced theta rhythm in hippocampal slices. Brain Res. 447,364-368.
Bliss, T. V. and Collingridge, G. L, 1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 361,31-39.
Blitzer, R. D., Gil, O. and Landau, E. M., 1990. Cholinergic stimulation enhances long-term potentiation in the CA1 region of rat hippocampus. Neurosci Lett. 119, 207-210.
Blokland, A., 1995. Acetylcholine: a neurotransmitter for learning and memory? Brain Res Brain Res Rev.21, 285-300.
Bourjeily, N. and Suszkiw, J. B., 1997. Developmental cholinotoxicity of lead: loss of septal cholinergic neurons and long-term changes in cholinergic innervation of the hippocampus in perinatally lead-exposed rats. Brain Res. 771, 319-328.
Busselberg, D., Evans, M. L., Rahmann, H. and Carpenter, D. O., 1991. Lead and zinc block a voltage-activated calcium channel of Aplysia neurons. J Neurophysiol. 65, 786-795.
Cohn, J. and Cory-Slechta, D. A., 1993. Subsensitivity of lead-exposed rats to the accuracy-impairing and rate-altering effects of MK-801 on a multiple schedule of repeated learning and performance. Brain Res. 600, 208-218.
Cole, A. E. and Nicoll, R. A., 1983. Acetylcholine mediates a slow synaptic potential in hippocampal pyramidal cells. Science. 221, 1299-1301.
Cory-Slechta, D. A., 1995. Relationships between lead-induced learning impairments and changes in dopaminergic, cholinergic, and glutamatergic neurotransmitter system functions. Annu Rev Pharmacol Toxicol. 35,391-415.
Cory-Slechta, D. A. and Pokora, M. J., 1995. Lead-induced changes in muscarinic cholinergic sensitivity. Neurotoxicology. 16, 337-347.
Coyle, J. T., Price, D. L. and DeLong, M. R., 1983. Alzheimer's disease: a disorder of cortical cholinergic innervation. Science. 219, 1184-1190.
Frotscher, M. and Leranth, C, 1985. 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.
Harvey, J., Balasubramaniam, R. and Collingridge, G L., 1993. Carbachol can potentiate N-methyl-D-aspartate responses in the rat hippocampus by a staurosporine and thapsigargin-insensitive mechanism. Neurosci Lett. 162, 165-168.
Hasselmo, M. E., 1999. Neuromodulation: acetylcholine and memory consolidation. Trends Cogn Sci. 3,351-359.
Herreras, O., Solis, J. M, Herranz, A. S., Martin del Rio, R. and Lerma, J., 1988. Sensory modulation of hippocampal transmission. II. Evidence for a cholinergic locus of inhibition in the Schaffer-CA1 synapse. Brain Res. 461, 303-313.
Konopacki, J., Bland, B. H. and Roth, S. H., 1988. Evidence that activation of in vitro hippocampal theta rhythm only involves muscarinic receptors. Brain Res. 455, 110-114.
Levey, A. I., Edmunds, S. M., Koliatsos, V., Wiley, R. G. and Heilman, C. J., 1995. Expression of m1-m4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulation by cholinergic innervation. J Neurosci. 15,4077-4092.
Lewis, P. R. and Shute, C. C, 1967. The cholinergic limbic system: projections to hippocampal formation, medial cortex, nuclei of the ascending cholinergic reticular system, and the subfornical organ and supra-optic crest. Brain. 90, 521-540.
Macadar, O., Roig, J. A., Monti, J. M. and Budelli, R., 1970. The functional relationship between septal and hippocampal unit activity and hippocampal theta rhythm. Physiol Behav. 5,1443-1449.
Madison, D. V., Lancaster, B. and Nicoll, R. A., 1987. Voltage clamp analysis of cholinergic action in the hippocampus. J Neurosci. 7, 733-741.
Marino, M. J., Rouse, S. T., Levey, A. I., Potter, L. T. and Conn, P. J., 1998. Activation of the genetically defined ml muscarinic receptor potentiates N-methyl-D-aspartate (NMDA) receptor currents in hippocampal pyramidal cells. Proc Natl Acad Sci U S A. 95,11465-11470.
McCormick, D. A. and Prince, D. A., 1986. Mechanisms of action of acetylcholine in the guinea-pig cerebral cortex in vitro. J Physiol. 375,169-194.
Nakajima, Y., Nakajima, S., Leonard, R. J. and Yamaguchi, K., 1986. Acetylcholine raises excitability by inhibiting the fast transient potassium current in cultured hippocampal neurons. Proc Natl Acad Sci U S A. 83, 3022-3026.
Nehru, B. and Sidhu, P., 2001. Behavior and neurotoxic consequences of lead on rat brain followed by recovery. Biol Trace Elem Res. 84,113-121.
Patil, M. M., Linster, C, Lubenov, E. and Hasselmo, M. E., 1998. Cholinergic agonist carbachol enables associative long-term potentiation in piriform cortex slices. J Neurophysiol. 80,2467-2474.
Qian, J. and Saggau, P., 1997. Presynaptic inhibition of synaptic transmission in the rat hippocampus by activation of muscarinic receptors: involvement of presynaptic calcium influx. Br J Pharmacol. 122,511-519.
Ruan, D. Y, Chen, J. T., Zhao, C, Xu, Y. Z., Wang, M. and Zhao, W. F., 1998. Impairment of long-term potentiation and paired-pulse facilitation in rat hippocampal dentate gyrus following developmental lead exposure in vivo. Brain Res. 806, 196-201.
Sui, L. and Ruan, D. Y, 2000. Impairment of the Ca2+-permeable AMPA/kainate receptors by lead exposure in organotypic rat hippocampal slice cultures. Pharmacol Toxicol. 87,204-210.
Toth, K. and McBain, C. J., 2000. Target-specific expression of pre- and postsynaptic mechanisms. J Physiol. 525 Pt 1, 41-51.
Ujihara, H., Sasa, M. and Ban, T, 1995. Selective blockade of P-type calcium channels by lead in cultured hippocampal neurons. Jpn J Pharmacol. 67, 267-269.
Williams, S. and Johnston, D., 1988. Muscarinic depression of long-term potentiation in CA3 hippocampal neurons. Science. 242, 84-87.
Winkler, J., Thai, L. J., Gage, F. H. and Fisher, L. J., 1998. Cholinergic strategies for Alzheimer's disease. J Mol Med. 76, 555-567.
Zhang, X. Y, Liu, A. P., Ruan, D. Y and Liu, J., 2002. Effect of developmental lead exposure on the expression of specific NMDA receptor subunit mRNAs in the hippocampus of neonatal rats by digoxigenin-labeled in situ hybridization histochemistry. Neurotoxicol Teratol. 24,149-160.
Zhao, W. F., Ruan, D. Y, Xu, Y Z., Chen, J. T., Wang, M. and Ge, S. Y, 1999. The effects of chronic lead exposure on long-term depression in area CA1 and dentate gyrus of rat hippocampus in vitro.Brain Res.818,153-159.
Zucker,R.S.,1989.Short-term synaptic plasticity.Annu P,ev Neurosci.12,13-31.
Zucker,R.S.,1999.Calcium- and activity-dependent synaptic plasticity.Curt Opin Neurobiol.9,305-313.
Alkondon M, Costa ACS, Radhakrishnan V, Aronstam RS, Albuquerque EX, Selective blockade of NMDA-activated channel currents may be implicated in learning deficits caused by lead. FEBS Lett (1990) 261:124-30
Altmann L, Impairment of long-term potentiation and learning following chronic lead exposure.Toxicol Lett (1993) 66:105-12
Altmann L, Impairment of long-term potentiation and learning following chronic lead exposure.Toxicol Lett (1993) 66:105-12
Altmann L, Sveinsson K, Wiegand H, Long-term potentiation in rat hippocampal slices is impaired following acute lead perfusion. Neurosci Lett (1991) 128:124-130
Ashby JAS, A neurological and biochemical study of early lead poisoning. Br J Ind (1980) 37:133-140.
Audesirk G, Electrophysiology of lead intoxication effects on voltage-sensitive ion channels.Newotoxicology (1993) 14: 137-147
Balbus-Kornfeld JM, Stewart W, Bolla KI, Schwartz BS, Cumulative exposure to inorganic lead and neurobehav ioral test performance in adults: an epidemiological review. Occup Enviro Med (1995)52:2-12
Bellinger DC, Leviton A, Waternaux C. Longitudinal analyses of prenatal and postnatal lead exposure and early cognitive development. N Engl J Med. (1987) 316:1037-43
Bellinger DC, Sloman J, Leviton A, Rabinowitz M. Low level exposure and children's cognitive function in the preschool years. Pediatrics (1991) 87: 219-227
Bellinger DC, Stilfs KM, Needleman HL, Low-level lead exposure, intelligence and academic achievement: a long-term follow-up study. Pediatrics, (1992) 90: 855-861
Bilsselberg D, Evans ML, Rahmann H, Carpenter DO, Lead and zinc block a voltage-activated calcium channel of Aplysia neurons. J. Neurophysiol. (1991) 65: 786-795.
Busselberg D, Platt B, Michael D, Carpenter DO, Mammalian voltage-activated calcium channel currents are blocked by Pb~(++)Zn~(++),and Al~(3+). J Neurophysiol (1994) 71: 234-245
Cantarow A, Trumper M, (1944) Lead poisoning. Baltimore, MD: Williams and Wilkins. Cory-Slechta D. MK-801 subsensitivity following postweaning lead exposure. Neurotoxicology (1995a) 16: 83-96
Cory-Slechta DA, Relationships between lead-induced learning impairments and changes in dopaminergic, cholinergic, and glutamatergic neurotransmitter system functions.Ann Rev Pharmacol Toxicol (1995b) 35: 391-415
Dai XQ, Ruan DY, Chen JT, Wang M, Cai L The effects of lead on transient outward currents of acutely dissociated rat dorsal root ganglion. Brain Res. (2001) 904:327-340
Davis JM, Svendsgaard DJ Nerve conduction velocity and lead: a critical review and meta-analysis. In Johnson BL (editors): Advances in Neurobehavioral Toxicology: Application in Enviromental and Occupational Health. Chelsea, Michigan: Lewis Publishers, (1990) p:353-376.
Ellen K, Silbergeld. Subcellular mechanisms of lead neurotoxicity. Brain Res (1978) 148:451-467
Feldman RG, Haddow J, Kopito L, Schwachman H, Altered peripheral nerve conduction velocity: chronic lead intoxication in children. Am JDis Child(1973) 125: 39-41.
Finkelstein Y, Mechanism of lead-induced neurotoxicity. Shaare Zedek Medical Center Fjerdingstad EJ, Hippocampus: Selective concentration of lead in the normal rat brain. Brain Res.(1974)80:350-354
Guilarte TR, Miceli RC, Age-dependent effects of lead on [3H]MK-801 binding to the NMDA receptor-gated ionophore: in vitro and in vivo studies. Neurosci Lett. (1992) 148:27-30
Haden ST, Brown EM, Stoll AL, Scott J, Fuleihan GE.The effect of lithium on calcium-induced changes in adrenocorticotrophin levels J Clin Endocrinol Metab (1999) 84:198-200
Hori N, Busselberg D. Matthew MR, Parsons PJ, Carpenter DO, Lead blocks LTP by an action not at NMDA receptors.Exp Neurol (1993) 119: 192-97
Lasley SM, Gilbert ME, Presynaptic glutamatergic function in dentate gyrus in vivo is dimished by chronic exposure to inorganic lead.Brain Res (1996) 736:125-34
Lasley SM, Polan-Curtain J, Armstrong DL, Chronic exposure to environmental levels of lead impairs in vivo induction of long-term potentiation. Brain Res (1993) 614: 347-51
Madeja M, Mubhoff U, Binding N, Witting U, Speckmann EJ, Effects of Pb~(2+) on delayed-rectifier potassium channels in acutely isolated hippocampal neurons. J. Neurophysiol.(1997)78: 2649-2654.
Markovac J, Goldstein GW, Picomolar concentrations of lead stimulate brain protein kinase C.Nature (1988)334: 71-73
Mayer ML, Westbrook GL, A voltage-clamp analysis of inward (anomalous) rectification in mouse spinal sensory ganglion neurons. J Physiol. (1983) 340: 19-45
Minnema DJ, Calcium influx and neurotransmitter release from rat hippocampal synaptosomes exposed to lead. Toxicol App Pharmacol (1988) 92: 351-57
Moriyoshi K, Masu M, Ishii T, Shigemoto R, Mizuno N, Nakanishi S, Molecular cloning and characterization of the rat NMDA receptor. Nature (1991) 354: 31-7.
Murata K, Araki S, Yokoyama K, Uchida E, Fujimura Y, Assessment of central, peripheral, and autonomic nervous system functions in lead workers: neuroelectrophysiological studies.Environ Res. (1993) 61: 323-336
Nathanson JA, Bloom FE, Lead-induced inhibition of brain adenyl cyclase. Nature (1975) 255:419-20
Needleman HL. Low-level lead exposure: the clinical implication of current research. (1989) Raven press New York
Pasternak G, Becker CE, Lash A, Bowler R, Estrin WJ, Law D, Cross-sectional neurotoxicology study of lead-exposed cohort. Clin Toxicol. (1989) 27: 37-51
Riess JA, Needleman HL, Cognitive, neural, behavioral effects of low-level lead exposure. The Vulnerable brain and environmental risks. (1992) Plenum press New York
Ruan DY, Chen JT.Zhao C. et al. Impairment of long-term potentiation and paired-pulse facilitation in rat hippocampal detate gyrus following developmental lead exposure in vivo.Brain Res (1998) 806:196-201.
Ruan DY, Yan KF, Ge SY et al. Effects of chronic lead exposure on short-term and long-term depression in area CAl of rat hippocampus in vivo. Chemosphere (2000) 41: 165-71.
Rubens O, Logina I, Kravale I, Eglite M, Donaghy M, Peripheral neuropathy in chronic occupational inorganic lead exposure: a clinical and electrophysiological study. J Newol Neurosurg Psychiatry. (2001) 71: 200-4.
Schwartz BS, Lee BK, Lee GS, Stewart WF, Lee SS, Hwang KY, Ahn KD, Kim YB, Bolla KI,Simon D, Parsons PJ, Todd AC, Associations of blood lead, dimercaptosuccinic acid-chelatable lead, and tibia lead with neurobehavioral test scores in South Korean lead workers.Am J Epidemiol. (2001) 153: 453-64.
Seppalainen AM, Hernberg S, Sensitive technique for detecting subclinical lead neuropathy. Br J Ind Med. (1972)29: 443-449
Shellenberger M, Effects of early lead exposure on neurotransmitter systems in the brain: a review with commentary. Neurotoxicol 1998,45: 117-22
Sierra EM, Rowles TK, Martin J- Bratton GR, Womac C, Low level lead neurotoxicity in a pregnant guinea pigs model: Nueroglial enzyme activities and brain trace metal concentrations Toxicology 1989, 59: 81-96
Sierra EM, Tiffany-Castiglioni E, Reduction of glutamine synthetase activity in astroglia exposed in culture to low level levels of inorganic lead.Toxicology 1991, 65: 295-304
Simons TJ Lead-calcium interactions in cellular lead toxicity. Neurotoxicology (1993) 14: 77-85.
Singer R, Valciukas JA, Lilis R, Lead exposure and nerve conduction velocity: the differential time course of sensory and motor nerve effects.Neurotoxicology(1983)4:193-202
Stoclet JC,Gerard D,Kilhoffer MC,Lugnier C,Miller R,Schaeffer P Calmodulin and its role in intracellular calcium regulation.Prog Neurobiol 1987,29:321-64
Stokes L,Letz R,Gerr F,Kolczak M,McNeill FE,Chettle DR,Kaye WE,Neurotoxicity in young adults 20 years after childhood exposure to lead:the Bunker Hill experience.Occup Environ Med.(1998)55:507-16.
Sui L,Ge SY,Ruan DY et al.Age-dependent impairment of long-term depression in area CA1and DG of rat hippocampus following developmental lead exposure in vitro.Neurotoxicol Teratol(2000)22:381-387.
Sui L,Ge SY,Ruan DY et al.Two components of long-term depression are impaired by chronic lead exposure in area CA1 and dentate gyms of rat hippocampus in vitro.Neurotoxicol Teratol (2000)2(5):741-9.
Talukder G,Harrison NL,On the mechanism of modulation of transient outward currents in cultured rat hippocampal neurons by di- and trivalent cations.J.Neurophisiol.(1995)73:73-79.
Tassler PL,Schwartz BS,Coresh J,Stewart WF,Todd AC,Associations of tibia lead,DMSA-chelatable lead,and blood lead with measures of peripheral nervous system function in former organolead manufacturing workers.American J.Ind Med.(2001)39:254-261.
Triebig G,Weltle D,Valentin H,Investigations on neurotoxicity of chemical substances at the workplace.Int Arch Occup Environ Health(1984)53:189-204.
Ujihara H,Sasa M,Ban T,Selective blockade of p-type calcium channels by lead in cultured hippocampal neurons.Jpn.J.Pharmacol.(1995)67:267-269
Wiegand H,Altmann L Neurophysiological aspects of hippocampal neurotoxicity.Neurotoxicology 1994,15:451-8
Xu YZ,Ruan DY,Wu Yet al.Nitric Oxide affects LTP in Area CA1 and CA3 of hippocampus in low-level lead exposed rat.Neurotoxicol Teratol(1998)20(1):69-73.
Yeh J,Chang Y,Wang J,Combined electroneurographic and electromyographic studies in lead workers.Occup Environ Med(1995)52:415-419.
Zimmerman-Tansella C,Campara P,D'Andrea F,Savonitto C,Tansella M,Psychological and physical complaints of subjects with low exposure to lead.Hum Toxicol.(1983)2:615-623.
何稼敏,铅的神经毒性作用机制。铅污染的危害与防治,P 184-7,香港新闻出版社(1997)。
陆巍,铅的神经毒作用机制。铅污染的危害与防治,P 40-42,香港新闻出版社(1997)。
阮迪云,陈聚涛,赵望发,柳素铃,顾炜玮,铅对海马齿状回L-LTP和双脉冲发应的影响.广东微量元素科学(1998)5:25-29
Abe K, Nakata A, Mizutani A, Saito H. 1994. Facilitatory but nonessential role of the muscarinic cholinergic system in the generation of long-term potentiation of population spikes in the dentate gyrus in vivo. Neuropharmacology 33(7):847-52.
Auerbach JM, Segal M. 1996. Muscarinic receptors mediating depression and long-term potentiation in rat hippocampus. J Physiol 492 (Pt 2):479-93.
Aura J, Sirvio J, Riekkinen P. 1997. Methoctramine moderately improves memory but pirenzepine disrupts performance in delayed non-matching to position test. European Journal of Pharmacology 333(2-3): 129-134.
Bartus RT, Dean RL, 3rd B, B., Lippa AS. 1982. The cholinergic hypothesis of geriatric memory dysfunction. Science 217:408-414.
Berkeley JL, Gomeza J, Wess J, Hamilton SE, Nathanson NM, Levey AI. 2001. M-l muscarinic acetylcholine receptors activate extracellular signal-regulated kinase in CA1 pyramidal neurons in mouse hippocampal slices. Molecular and Cellular Neuroscience 18(5):512-524.
Bliss TVP, Collingridge GL. 1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
Blitzer RD, Gil O, Landau EM. 1990. Cholinergic stimulation enhances long-term potentiation in the CA1 region of rat hippocampus. Neurosci Lett 119(2):207-10.
Boddeke EW, Enz A, Shapiro G. 1992. SDZ ENS 163, a selective muscarinic Ml receptor agonist, facilitates the induction of long-term potentiation in rat hippocampal slices. Eur J Pharmacol 222(1):21-5.
Burgard EC, Sarvey JM. 1990. Muscarinic receptor activation facilitates the induction of long-term potentiation (LTP) in the rat dentate gyrus. Neurosci Lett 116(l-2):34-9.
Coyle JT, Price DL, DeLong MR. 1983. Alzheimer's disease: a disorder of cortical cholinergic innervation. Science 219(4589): 1184-90.
Hajos N, Papp EC, Acsady L, Levey AI, Freund TF. 1998. Distinct interneuron types express m2 muscarinic receptor immunoreactivity on their dendrites or axon terminals in the hippocampus. Neuroscience 82(2):355-76.
Hamilton SE, Nathanson NM. 2001. The Ml receptor is required for muscarinic activation of mitogen-activated protein (MAP) kinase in murine cerebral cortical neurons. J Biol Chem 276(19):15850-3.
Harvey J, Balasubramaniam R, Collingridge GL. 1993. Carbachol can potentiate N-methyl-d-aspartate responses in the rat hippocampus by a staurosporine and thapsigargin-insensitive mechanism. Neurosci. Lett 162:165-168.
Hori H, Haruta K, Nanki M, Sakamoto N, Uemura K, Matsubara T, Itoh K, Iguchi A. 1995.Pressor-Response Induced by the Hippocampal Administration of Neostigmine Is Suppressed by Ml Muscarinic Antagonist. Life Sciences 57(20): 1853-1859.
Inglis FM, Fibiger HC. 1995. Increases in hippocampal and frontal cortical acetylcholine release associated with presentation of sensory stimuli. Neuroscience 66(1 ):81 -6.
Jacob SN. Choe C-U, Uhlen P, Degray B, Yeckel MF, Ehrlich BE. 2005. Signaling microdomains regulate inositol 1,4,5-trisphosphate-mediated intracellular calcium transients in cultured neurons. The Journal of Neuroscience 25:2853-2864.
Jerusalinsky D, Kornisiuk E, Izquierdo I. 1997. Cholinergic neurotransmission and synaptic plasticity concerning memory processing. Neurochem. Res 22:507-515.
Levey AI. 1996. Muscarinic acetycholine receptor expression in memory circuits: implications for treatment of Alzheimer disease. Proc.Natl.Acad.sci.USA 93:13541-13546.
Levey AI, Edmunds SM, Koliatsos VK, Wiley RG, Heilman CJ. 1995. Expression of m1-m4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulation by cholinergic innervation. The Journal of Neuroscience 15:4077-4092.
Levey AI, Kitt C A. Simonds WF, Price DL, Brann MR. 1991. Identification and localization of muscarinic acetylcholine receptor protein in brain with subtype-specific antibodies. J.Neurosci 11:3218-3226.
Li S, Cullen WK, Anwyl R, Rowan MJ. 2007. Muscarinic acetylcholine receptor-dependent induction of persistent synaptic enhancement in rat hippocampus in vivo. Neuroscience 144(2):754-61.
Madison DV, Lancaster B, Nicoll RA. 1987. Voltage clamp analysis of cholinergic action in the hippocampus. J. Neurosci 7:733-741.
Mastropaolo J, Nadi NS, Ostrowski NL, Crawley JN. 1988. Galanin antagonizes acetylcholine on a memory task in basal forebrain-lesioned rats. Proc Natl Acad Sci U S A 85(24):9841-5.
Messer WS, Bohnett M, Stibbe J. 1990. Evidence for a Preferential Involvement of Ml Muscarinic Receptors in Representational Memory. Neuroscience Letters 116(1-2):184-189.
Mesulam MM, Mufson EJ, Wainer BH, Levey AI. 1983. Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Chl-Ch6). Neuroscience 10:1185-1201.
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(5):1267-75.
Patil MM, Linster C, Lubenov E, Hasselmo ME. 1998. Cholinergic agonist carbachol enables associative long-term potentiation in piriform cortex slices. J Neurophysiol 80(5):2467-74.
Rouse ST, Edmunds SM, Yi H, Gilmor ML, Levey AI. 2000. Localization of M(2) muscarinic acetylcholine receptor protein in cholinergic and non-cholinergic terminals in rat hippocampus. Neurosci Lett 284(3): 182-6.
Saito K, Yoshioka M, Kohya T, Kitabatake A. 1994. Involvement of Muscarinic Ml Receptor in the Central Pathway of the Serotonin-Induced Bezold-Jarisch Reflex in Rats. Journal of the Autonomic Nervous System 49(l):61-68.
Segal M, Auerbach JM. 1997. Muscarinic receptors involved in hippocampal plasticity. Life Sci.60:1085-1091.
Shimoshige Y, Maeda T, Kaneko S, Akaike A, Satoh M. 1997. Involvement of M2 receptor in an enhancement of long-term potentiation by carbachol in Schaffer collateral-CAl synapses of hippocampal slices. Neuroscience Research 27:175-180.
Shinoe T, Matsui M, Taketo MM, Manabe T. 2005. Modulation of synaptic plasticity by physiological activation of Ml muscarinic acetylcholine receptors in the mouse hippocampus. J Neurosci 25(48): 11194-200.
Winkler J, Thal LJ, Gage FH, Fisher LJ. 1998. Cholinergic strategies for Alzheimer's disease. J Mol Med 76(8):555-67.
Adhami, V. M., Husain, R., Agarwal, A. K. and Seth, P. K., 2000. Intrahippocampal cholinergic-rich transplants restore lead-induced deficits: a preliminary study in rats.Neurotoxicol Teratol. 22,41-53.
Aigner, T. G, 1995. Pharmacology of memory: cholinergic-glutamatergic interactions. Curr Opin Neurobiol.5,155-160.
Alkondon, M., Costa, A. C, Radhakrishnan, V., Aronstam, R. S. and Albuquerque, E. X., 1990.Selective blockade of NMDA-activated channel currents may be implicated in learning deficits caused by lead. FEBS Lett. 261, 124-130.
Alkondon, M., Pereira, E. F., Barbosa, C. T. and Albuquerque, E. X., 1997. Neuronal nicotinic acetylcholine receptor activation modulates gamma-aminobutyric acid release from CAI neurons of rat hippocampal slices. J Pharmacol Exp Ther. 283,1396-1411.
Auerbach, J. M. and Segal, M., 1994. A novel cholinergic induction of long-term potentiation in rat hippocampus. J Neurophysiol. 72, 2034-2040.
Auerbach, J. M. and Segal, M., 1996. Muscarinic receptors mediating depression and long-term potentiation in rat hippocampus. J Physiol. 492 (Pt 2), 479-493.
Bartus, R. T., Dean, R. L., 3rd, Beer, B. and Lippa, A. S., 1982. The cholinergic hypothesis of geriatric memory dysfunction. Science. 217, 408-414.
Benardo, L. S. and Prince, D. A., 1982. Cholinergic excitation of mammalian hippocampal pyramidal cells. Brain Res. 249, 315-331.
Blitzer, R. D., Gil, O. and Landau, E. M., 1990. Cholinergic stimulation enhances long-term potentiation in the CAI region of rat hippocampus. Neurosci Lett. 119,207-210.
Braga, M. F., Pereira, E. F. and Albuquerque, E. X., 1999. Nanomolar concentrations of lead inhibit glutamatergic and GABAergic transmission in hippocampal neurons. Brain Res. 826,22-34.
Buckley, N. J., Bonner, T. I. and Brann, M. R., 1988. Localization of a family of muscarinic receptor mRNAs in rat brain. J Neurosci. 8, 4646-4652.
Busselberg, D., Evans, M. L., Rahmann, H. and Carpenter, D. O., 1991. Lead and zinc block a voltage-activated calcium channel of Aplysia neurons. J Neurophysiol. 65, 786-795.
Conn, J. and Cory-Slechta, D. A., 1993. Subsensitivity of lead-exposed rats to the accuracy-impairing and rate-altering effects of MK-801 on a multiple schedule of repeated learning and performance. Brain Res. 600,208-218.
Cory-Slechta, D. A. and Pokora, M. J., 1995. Lead-induced changes in muscarinic cholinergic sensitivity. Neurotoxicology. 16, 337-347.
Coyle, J. T., Price, D. L. and DeLong, M. R., 1983. Alzheimer's disease: a disorder of cortical cholinergic innervation. Science. 219,1184-1190.
de Sevilla, D. F., Cabezas, C, de Prada, A. N., Sanchez-Jimenez, A. and Buno, W., 2002. Selective muscarinic regulation of functional glutamatergic Schaffer collateral synapses in rat CAl pyramidal neurons. J Physiol. 545, 51-63.
Dudar, J. D., 1977. The role of the septal nuclei in the release of acetyl-choline from the rabbit cerebral cortex and dorsal hippocampus and the effect of atropine. Brain Res. 129,237-246.
Frotscher, M. and Leranth, C, 1985. 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.
Frotscher, M., Vida, I. and Bender, R., 2000. Evidence for the existence of non-GABAergic,cholinergic interneurons in the rodent hippocampus. Neuroscience. 96,27-31.
Gaztelu, J. M. and Buno, W., Jr., 1982. Septo-hippocampal relationships during EEG theta rhythm. Electroencephalogr Clin Neurophysiol. 54,375-387.
Goda, Y. and Stevens, C. F., 1996. Synoptic plasticity: the basis of particular types of learning.CurrBiol.6, 375-378.
Hamill, O. P., Marty, A., Neher, E., Sakmann, B. and Sigworth, F. J., 1981. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches.Pflugers Arch.391,85-100.
Harvey, J., Balasubramaniam, R. and Collingridge, G. L., 1993. Carbachol can potentiate N-methyl-D-aspartate responses in the rat hippocampus by a staurosporine and thapsigargin-insensitive mechanism. Neurosci Lett. 162, 165-168.
Hasselmo, M. E., 1999. Neuromodulation: acetylcholine and memory consolidation. Trends Cogn Sci.3, 351-359.
Hefft, S., Hulo, S., Bertrand, D. and Muller, D., 1999. Synaptic transmission at nicotinic acetylcholine receptors in rat hippocampal organotypic cultures and slices. J Physiol. 515 ( Pt 3), 769-776.
Hersch, S. M., Gutekunst, C. A., Rees, H. D., Heilman, C. J. and Levey, A. I., 1994. Distribution of m1-m4 muscarinic receptor proteins in the rat striatum: light and electron microscopic immunocytochemistry using subtype-specific antibodies. J Neurosci. 14,3351-3363.
Hersch, S. M. and Levey, A. I., 1995. Diverse pre- and post-synaptic expression of m1-m4 muscarinic receptor proteins in neurons and afferents in the rat neostriatum. Life Sci. 56,931-938.
Hounsgaard, J., 1978. Presynaptic inhibitory action of acetylcholine in area CAI of the hippocampus. Exp Neurol. 62, 787-797.
Huerta, P. T. and Lisman, J. E., 1995. Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CAI in vitro. Neuron. 15, 1053-1063.
Hwang, T. N. and Copenhagen, D. R., 1999. Automatic detection, characterization, and discrimination of kinetically distinct spontaneous synaptic events. J Neurosci Methods. 92,65-73.
Iga, Y., Arisawa, H., Ise, M., Yasuda, H. and Takeshita, Y., 1996. Modulation of rhythmical slow activity, long-term potentiation and memory by muscarinic receptor agonists. Eur J Pharmacol.308,13-19.
Jett, D. A. and Guilarte, T. R., 1995. Developmental lead exposure alters N-methyl-D-aspartate and muscarinic cholinergic receptors in the rat hippocampus: an autoradiographic study.Neurotoxicology. 16, 7-18.
Lewis, P. R. and Shute, C. C, 1967. The cholinergic limbic system: projections to hippocampal formation, medial cortex, nuclei of the ascending cholinergic reticular system, and the subfornical organ and supra-optic crest. Brain. 90, 521-540.
Macadar, O., Roig, J. A., Monti, J. M. and Budelli, R., 1970. The functional relationship between septal and hippocampal unit activity and hippocampal theta rhythm. Physiol Behav. 5,1443-1449.
Madison, D. V., Lancaster, B. and Nicoll, R. A., 1987. Voltage clamp analysis of cholinergic action in the hippocampus. J Neurosci. 7, 733-741.
Madison, D. V, Malenka, R. C. and Nicoll, R. A., 1991. Mechanisms underlying long-term potentiation of synaptic transmission. Annu Rev Neurosci. 14, 379-397.
Marino, M. J., Rouse, S. T., Levey, A. I., Potter, L. T. and Conn, P. J., 1998. Activation of the genetically defined ml muscarinic receptor potentiates N-methyl-D-aspartate (NMDA) receptor currents in hippocampal pyramidal cells. Proc Natl Acad Sci U S A. 95,11465-11470.
Mazzolini, M., Traverso, S. and Marchetti, C, 2001. Multiple pathways of Pb(2+) permeation in rat cerebellar granule neurones. J Neurochem. 79, 407-416.
Minnema, D. J., Michaelson, I. A. and Cooper, G. P., 1988. Calcium efflux and neurotransmitter release from rat hippocampal synaptosomes exposed to lead. Toxicol Appl Pharmacol. 92,351-357.
Patil, M. M, Linster, C, Lubenov, E. and Hasselmo, M. E., 1998. Cholinergic agonist carbachol enables associative long-term potentiation in piriform cortex slices. J Neurophysiol. 80,2467-2474.
Qian, J. and Saggau, P., 1997. Presynaptic inhibition of synaptic transmission in the rat hippocampus by activation of muscarinic receptors: involvement of presynaptic calcium influx.Br J Pharmacol. 122,511-519.
Richter, M., Schilling, T. and Muller, W., 1999. Muscarinic control of intracortical connections to layer II in rat entorhinal cortex slice. Neurosci Lett. 273, 200-202.
Ruan, D. Y., Chen, J. T., Zhao, C, Xu, Y. Z., Wang, M. and Zhao, W. F., 1998. Impairment of long-term potentiation and paired-pulse facilitation in rat hippocampal dentate gyrus following developmental lead exposure in vivo. Brain Res. 806,196-201.
Ruan, D. Y, Yan, K. F., Ge, S. Y., Xu, Y. Z., Chen, J. T. and Wang, M., 2000. Effects of chronic lead exposure on short-term and long-term depression in area CAl of the rat hippocampus in vivo. Chemosphere. 41,165-171.
Silbergeld, E. K. and Adler, H. S., 1978. Subcellular mechanisms of lead neurotoxicity. Brain Res.148,451-467.
Toth, K. and McBain, C. J., 2000. Target-specific expression of pre- and postsynaptic mechanisms.J Physiol. 525 Pt1,41-51.
Uteshev, V, Busselberg, D. and Haas, H. L., 1993. Pb2+ modulates the NMDA-receptor-channel complex. Naunyn Schmiedebergs Arch Pharmacol. 347,209-213.
Valentino, R. J. and Dingledine, R., 1981. Presynaptic inhibitory effect of acetylcholine in the hippocampus. J Neurosci. 1, 784-792.
Van der Kloot, W, 1989. Statistical and graphical methods for testing the hypothesis that quanta are made up of subunits. J Neurosci Methods. 27, 81-89.
Wei, J., Walton, E. A., Milici, A. and Buccafusco, J. J., 1994. m1-m5 muscarinic receptor distribution in rat CNS by RT-PCR and HPLC. J Neurochem. 63,815-821.
Winkler, J., Thal, L. J., Gage, F. H. and Fisher, L. J., 1998. Cholinergic strategies for Alzheimer's disease. J Mol Med. 76, 555-567.
Xu, Y. Z., Ruan, D. Y., Wu, Y, Jiang, Y. B., Chen, S. Y, Chen, J. and Shi, P., 1998. Nitric oxide affects LTP in area CAl and CA3 of hippocampus in low-level lead-exposed rat. Neurotoxicol Teratol. 20,69-73.
Yun, S. H., Cheong, M. Y, Mook-Jung, I., Huh, K., Lee, C. and Jung, M. W., 2000. Cholinergic modulation of synaptic transmission and plasticity in entorhinal cortex and hippocampus of the rat. Neuroscience. 97, 671-676.
Zhang, L. and Warren, R. A., 2002. Muscarinic and nicotinic presynaptic modulation of EPSCs in the nucleus accumbens during postnatal development. J Neurophysiol. 88, 3315-3330.
Zhao, W. F., Ruan, D. Y, Xu, Y. Z., Chen, J. T., Wang, M. and Ge, S. Y, 1999. The effects of chronic lead exposure on long-term depression in area CAl and dentate gyrus of rat hippocampus in vitro. Brain Res. 818,153-159.
Zucker, R. S., 1989. Short-term synaptic plasticity. Annu Rev Neurosci. 12,13-31.
Zucker, R. S., 1999. Calcium- and activity-dependent synaptic plasticity. Curr Opin Neurobiol. 9,305-313.
Abeliovich A, Coan C, Goda Y et al. Modified hippocampal long-term potentiation in γ-PKC mutant mice. Cell (1993) 75:1253-1262.
Alford S, Frengurli BG, Schofield JG et al. Characterization of Ca~(2+) signals induced in hippocampal CA1 neurons by synaptic activation of NMDA receptors. J Physiol (London) (1993)469: 693-716.
Bashir ZI, Jane DE, Sunter DC et al. Metabotropic glutamate receptors contribute to the induction of long-term depression in the CA1 region of the hippocampus. Eur J Pharmacol (1993)239: 265-266.
Bear MF, Dudek SM and Gold JT. Homosynaptic long-term depression in CA1 of rat hippocampus in vitro. Soc Neurosci Abstr (1992) 17: 533P.
Berger TW. Long-term potentiation of hippocampal synaptic transmission affects rate of behavioral learning. Science (1984) 224: 627-630.
Bliss TV. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol (1973) 232:331-356.
Bliss TV and Collibgridge GL. A synaptic model of memory: long-term potentiation in the hippocampus. Nature (1993) 361: 31-39.
Bolshakov VY and Siegelbaum SA. Postsynaptic induction and pre-synaptic expression of hippocampal long-term depression. Science (1994) 264: 1148-1152.
Christie BR, Kerr DS and Abraham WC. The flip side of synaptic plasticity: long-term depression mechanisms in the hippocampus. Hippocampus (1994) 4: 127-135.
Cummings JA, Nicolas SM and Malenka RC. Induction in the rat hippocampus of long-term potentiation(LTP) and long-term depression(LTD) in the presence of nitric oxide synthase inhibitor. Neurosci Lett (1994) 176: 110-114.
Duvoisin RM, Zhang C and Ramonell K. A novel metabotropic glutamate receptor expressed in the retina and olfatory bulb. J Neurosci (1995) 15: 3075-3083.
Dudek SM and Bear MF. Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J Neurosci (1993) 13: 2910-2918.
Dunwiddie T and Lynch G Long-term potentiation and depression of synaptic responses in the rat hippocampus: location, frequency dependency. J Physiol (London) (1978) 276: 353-367.
Fleischer S and Inui M. Biochemistry and biophysics of excitation- contraction coupling. Ann Rev Biophys Biophys Chem (1989) 18: 333-364.
Galione A, White A, Willmot N et al. cGMP mobilizes intracellular Ca2+ in sea urchin eggs by stimulating cyclic ADP-ribose synthesis. Nature (1993) 365: 456-459.
Griffith WH. Voltage-clamp analysis of posttetanic potentiation of mossy fiber to CA3 synapse in hippocampus. J Neurophysiol (1990) 63: 491-501.
Hebb DO. The organization of behavior. Wiley, New York (1949).
Izumi Y and Zorumski CF. Nitric oxide and long-term synaptic depression in the rat hippocampus. Neuroreport (1993) 4: 1131-1134.
Kirkwood A, Aizenman CD and Bear MF. Common forms of plasticity in hippocampus and visual cortex in vitro. Soc Neurosci Abstr (1994) 18: 1499.
Kirkwood A and Bear MF. Homosynaptic long-term depression in the visual cortex. J Neurosci (1994) 14: 3404-3412.
Kobayashi K, Manabe T and Takahashi T. Presynaptic long-term depression at the hippocampal mossy fiber-CA3 synapse. Science 273: 648—650.
Linden DJ and Connor JA. Long-term depression. Ann Rev Neurosci (1995) 18: 319-357.
Lisman J. A mechanism for the Hebb and the anti-Hebb process underlying learning and memory.Proc Natl Acad Sci USA (1989) 86: 9574-9578.
Phelps ME. An investigation of a double-tracer technique for positron computerized tomography.J Nucl Med(1982)23: 816-822.
Malenka RC, Lancaster B and Zucker RS. Temporal limits on the rise in postsynaptic calcium required for the induction of long-term potentiation. Neuron (1993) 9: 121-128.
Manahan-Vaughan D. Group 1 and 2 metabotropic glutamate receptor play differential roles in hippocampal long-term depression and long-term potentiation in freely moving rats. J Neurosci (1997) 17(9): 3303-3311.
Masu M. Tanabe Y. Tsuchida K et al. Sequence and expression of a metabotropic glutamate receptor. Nature (1991) 349: 760-765.
McPherson PS and Kim YK. The brain ryanodine receptor: a caffeine- sensitive calcium release channel. Neuron (1991) 7: 17-75.
Meszaros LG. Bak J and Chu A. Cyclic ADP-ribose as an endogenous regulator of the non-skeletal type ryanodine receptor Ca2+ channel. Nature (1993) 364: 76-79.
Miyakawa H, Ross WN, Jaffe DB et al. Synaptically activated increases in Ca2+ concentration in hippocampal pyramidal cells are primarily due to voltage-gated Ca2+ channels. Neuron (1992) 9: 1163-1173.
Monaghan D. Distribution of NMD A-sensitive L-[3H] glutamate-binding sites in rat brain. J Neurosci(1987) 329: 724-726.
Mulkey RM and Malenka RC. Mechanisms underlying inductionof homosynaptic long-term depression in area CA1 of the hippocampus. Neuron (1992) 9: 967-975.
Muller W and Connor JA. Synaptic Ca2+ responses in dendritic spines: the spine as an individual neuronal compartment. Nature (1991) 354: 73-76.
Mulkey RM. Herron CE and Malenka RC. An essential role for protein phosphatases in hippocampal long-term depression. Science (1993) 261: 1051-1055.
Nakajima Y. Iwakabe H, Akazawa C et al. Molecular of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-amino-4-phosphonobutyrate. J Biol Chem (1993) 268: 11868-11873.
O'Dell TJ and Kandel ER. Low-frequency stimulation erases LTP through an NMDA receptor-mediated activation of protein phosphatases. Leam Mem (1994) 1: 129-139.
Okamoto Ni Horis S. Akazawa C et al. Molecular characterization of a novel metabotropic glutamate receptor mGluR7 coupled to inhibitory cyclic AMP signal transduction. J Biol Chem (1994) 269: 1231-1236.
O'Mara SM, Rowan MJ and Anwyl R. Dantrolene inhibits long-term depression and depotentiation of synaptic transmission in the rat dentate gyrus. Neuroscience (1995) 68:621-624.
O'Mara SM, Rowan MJ and Anwyl R. Metabotropic glutamate receptor-induced long-term depression and depotentiation in the dentate gyrus of the rat hippocampus in vitro.Neuropharmacology(1995)34: 983-989.
Perkel DJ, Petrozzino JJ. Nicoll RA et al. The role of Ca2+ entry via synaptically activated NMDA receptors in the induction of long-term potentiation. Neuron (1993) 11: 817-823.
Pozzo-Miller LD, Petrozzino JJ, Mahanty NK et al. Optical imaging of cytosolic calcium,electrophysiology, and ultrastructure in pyramidal neurons of organotypic slice cultures from rat hippocampus. Neuroimage (1993) 1: 109-20
Racine RJ. Milgram NW and Hafner S. Long-term potentiation phenomena in the rat limbic forebrain. Brain Res (1983) 260: 217-232.
Regehr WG. Connor JA and Tank DW. Optical imaging of calcium accumulation in hippocampal pyramidal cells during synaptic activation. Nature (1989) 341: 533-536.
Regehr WG and Tank DW. Calcium concentration dynamics produced by synaptic activation of CA1 hippocampal pyramidal cells. J Neurosci (1992) 12: 4202-4223.
Reyes M and Stanton PK.Induction of hippocampal long-term depression required release of Ca2+ from separate presynaptic and postsynaptic intracellular stores.J Neurosci(1996)16(19):5951-5960.
Robinson GB and Racine RJ.Heterosynaptic interactions between septal and entorhinai inputs to the dentate gyrus:long-term potentiation effects.Brain Res(1982)249:162-166.
Schuman FM,Meffert MK,Schulman H et al.An ADP-ribosyltransferase as a potential target for nitric oxide action in hippocampal long-term potentiation.Proc Natl Acad Sci USA(1994)91:11958-11962.
Scoville WB and Milner B.Loss of recent memory after bilateral hippocampal lesions.J Neurol Neurosurg Psych(1957)20:11-21.
Selig DK,Lee HK,Bear MF et al.Reexamination of the effects of MCPG on hippocampal LTP,LTD,and depotentiation.J Neurophysiol(1995)74:1075-1082.
Stevens CF and Wang Y.Reversal of long-term potentiation by inhibitor of haem oxygenase.Nature(1993)364:147-149.
Tanabe Y,Masu M,Ishii T et al.A family of metabotropic glutamate receptors.Neuron(1992)8:169-179.
Tanabe Y,Normura A,Masu M et al.Signal transduction,pharmacological properties,and expression patterns of two rat metabotropic glutamate receptors,mGluR3 and mGluR4.J Neurosci(1993)13:1372-1378.
Tsumoto T.Long-term depression in cerebral cortex:a possible substrate of "forgetting" that should not be forgotten.Neurosci Res(1993)16:263-270.
Vincent SR.Neurons that say NO.TINS(1992)15:108-113.
Wang Y,Rowan MJ and Anwyl R.Induction of LTD in the dentate gyrus in vitro is NMDA receptor independent but dependent on Ca2+ influx via low-voltage-activated Ca2+ channel and release of Ca2+ from intracellular stores.J Neurophysiology(1997)77:812-825.
Yokoi M,Kobayashi K,Manabe T et al.Impairment of hippocampal mossy fiber LTD in mice lacking mGluR2.Science(1996)273:645P.
Zorumski CF and Izumi Y,Nitric oxide and hippocampal synaptic plasticity.BioChem Pharmacol(1993)46:477-485.
韩太真,关于长时程增强形成机制的研究进展.生理科学进展.(1994)25:60-63
韩太真、吴馥梅主编,学习与记忆的神经生物学 北京医科大学、中国协和大学联合出版社,(1998).
Alkondon, M., Pereira, E. F., Barbosa, C. T. and Albuquerque, E. X., 1997. Neuronal nicotinic acetylcholine receptor activation modulates gamma-aminobutyric acid release from CA1 neurons of rat hippocampal slices. J Pharmacol Exp Then 283,1396-1411.
Altmann, L., Weinsberg, F., Sveinsson, K., Lilienthal, H., Wiegand, H. and Winneke, G, 1993.Impairment of long-term potentiation and learning following chronic lead exposure.Toxicol Lett. 66, 105-112.
Auerbach, J. M. and Segal, M., 1994. A novel cholinergic induction of long-term potentiation in rat hippocampus. J Neurophysiol. 72,2034-2040.
Bartus, R. T., Dean, R. L., 3rd, Beer, B. and Lippa, A. S., 1982. The cholinergic hypothesis of geriatric memory dysfunction. Science. 217,408-414.
Benardo, L. S. and Prince, D. A., 1982. Cholinergic excitation of mammalian hippocampal pyramidal cells. Brain Res. 249,315-331.
Bielarczyk, H., Tomsig, J. L. and Suszkiw, J. B., 1994. Perinatal low-level lead exposure and the septo-hippocampal cholinergic system: selective reduction of muscarinic receptors and cholineacetyltransferase in the rat septum. Brain Res. 643, 211 -217.
Bland, B. H., Colom, L. V., Konopacki, J. and Roth, S. H., 1988. Intracellular records of carbachol-induced theta rhythm in hippocampal slices. Brain Res. 447,364-368.
Bliss, T. V. and Collingridge, G. L, 1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 361,31-39.
Blitzer, R. D., Gil, O. and Landau, E. M., 1990. Cholinergic stimulation enhances long-term potentiation in the CA1 region of rat hippocampus. Neurosci Lett. 119, 207-210.
Blokland, A., 1995. Acetylcholine: a neurotransmitter for learning and memory? Brain Res Brain Res Rev.21, 285-300.
Bourjeily, N. and Suszkiw, J. B., 1997. Developmental cholinotoxicity of lead: loss of septal cholinergic neurons and long-term changes in cholinergic innervation of the hippocampus in perinatally lead-exposed rats. Brain Res. 771, 319-328.
Busselberg, D., Evans, M. L., Rahmann, H. and Carpenter, D. O., 1991. Lead and zinc block a voltage-activated calcium channel of Aplysia neurons. J Neurophysiol. 65, 786-795.
Cohn, J. and Cory-Slechta, D. A., 1993. Subsensitivity of lead-exposed rats to the accuracy-impairing and rate-altering effects of MK-801 on a multiple schedule of repeated learning and performance. Brain Res. 600, 208-218.
Cole, A. E. and Nicoll, R. A., 1983. Acetylcholine mediates a slow synaptic potential in hippocampal pyramidal cells. Science. 221, 1299-1301.
Cory-Slechta, D. A., 1995. Relationships between lead-induced learning impairments and changes in dopaminergic, cholinergic, and glutamatergic neurotransmitter system functions. Annu Rev Pharmacol Toxicol. 35,391-415.
Cory-Slechta, D. A. and Pokora, M. J., 1995. Lead-induced changes in muscarinic cholinergic sensitivity. Neurotoxicology. 16, 337-347.
Coyle, J. T., Price, D. L. and DeLong, M. R., 1983. Alzheimer's disease: a disorder of cortical cholinergic innervation. Science. 219, 1184-1190.
Frotscher, M. and Leranth, C, 1985. 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.
Harvey, J., Balasubramaniam, R. and Collingridge, G L., 1993. Carbachol can potentiate N-methyl-D-aspartate responses in the rat hippocampus by a staurosporine and thapsigargin-insensitive mechanism. Neurosci Lett. 162, 165-168.
Hasselmo, M. E., 1999. Neuromodulation: acetylcholine and memory consolidation. Trends Cogn Sci. 3,351-359.
Herreras, O., Solis, J. M, Herranz, A. S., Martin del Rio, R. and Lerma, J., 1988. Sensory modulation of hippocampal transmission. II. Evidence for a cholinergic locus of inhibition in the Schaffer-CA1 synapse. Brain Res. 461, 303-313.
Konopacki, J., Bland, B. H. and Roth, S. H., 1988. Evidence that activation of in vitro hippocampal theta rhythm only involves muscarinic receptors. Brain Res. 455, 110-114.
Levey, A. I., Edmunds, S. M., Koliatsos, V., Wiley, R. G. and Heilman, C. J., 1995. Expression of m1-m4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulation by cholinergic innervation. J Neurosci. 15,4077-4092.
Lewis, P. R. and Shute, C. C, 1967. The cholinergic limbic system: projections to hippocampal formation, medial cortex, nuclei of the ascending cholinergic reticular system, and the subfornical organ and supra-optic crest. Brain. 90, 521-540.
Macadar, O., Roig, J. A., Monti, J. M. and Budelli, R., 1970. The functional relationship between septal and hippocampal unit activity and hippocampal theta rhythm. Physiol Behav. 5,1443-1449.
Madison, D. V., Lancaster, B. and Nicoll, R. A., 1987. Voltage clamp analysis of cholinergic action in the hippocampus. J Neurosci. 7, 733-741.
Marino, M. J., Rouse, S. T., Levey, A. I., Potter, L. T. and Conn, P. J., 1998. Activation of the genetically defined ml muscarinic receptor potentiates N-methyl-D-aspartate (NMDA) receptor currents in hippocampal pyramidal cells. Proc Natl Acad Sci U S A. 95,11465-11470.
McCormick, D. A. and Prince, D. A., 1986. Mechanisms of action of acetylcholine in the guinea-pig cerebral cortex in vitro. J Physiol. 375,169-194.
Nakajima, Y., Nakajima, S., Leonard, R. J. and Yamaguchi, K., 1986. Acetylcholine raises excitability by inhibiting the fast transient potassium current in cultured hippocampal neurons. Proc Natl Acad Sci U S A. 83, 3022-3026.
Nehru, B. and Sidhu, P., 2001. Behavior and neurotoxic consequences of lead on rat brain followed by recovery. Biol Trace Elem Res. 84,113-121.
Patil, M. M., Linster, C, Lubenov, E. and Hasselmo, M. E., 1998. Cholinergic agonist carbachol enables associative long-term potentiation in piriform cortex slices. J Neurophysiol. 80,2467-2474.
Qian, J. and Saggau, P., 1997. Presynaptic inhibition of synaptic transmission in the rat hippocampus by activation of muscarinic receptors: involvement of presynaptic calcium influx. Br J Pharmacol. 122,511-519.
Ruan, D. Y, Chen, J. T., Zhao, C, Xu, Y. Z., Wang, M. and Zhao, W. F., 1998. Impairment of long-term potentiation and paired-pulse facilitation in rat hippocampal dentate gyrus following developmental lead exposure in vivo. Brain Res. 806, 196-201.
Sui, L. and Ruan, D. Y, 2000. Impairment of the Ca2+-permeable AMPA/kainate receptors by lead exposure in organotypic rat hippocampal slice cultures. Pharmacol Toxicol. 87,204-210.
Toth, K. and McBain, C. J., 2000. Target-specific expression of pre- and postsynaptic mechanisms. J Physiol. 525 Pt 1, 41-51.
Ujihara, H., Sasa, M. and Ban, T, 1995. Selective blockade of P-type calcium channels by lead in cultured hippocampal neurons. Jpn J Pharmacol. 67, 267-269.
Williams, S. and Johnston, D., 1988. Muscarinic depression of long-term potentiation in CA3 hippocampal neurons. Science. 242, 84-87.
Winkler, J., Thai, L. J., Gage, F. H. and Fisher, L. J., 1998. Cholinergic strategies for Alzheimer's disease. J Mol Med. 76, 555-567.
Zhang, X. Y, Liu, A. P., Ruan, D. Y and Liu, J., 2002. Effect of developmental lead exposure on the expression of specific NMDA receptor subunit mRNAs in the hippocampus of neonatal rats by digoxigenin-labeled in situ hybridization histochemistry. Neurotoxicol Teratol. 24,149-160.
Zhao, W. F., Ruan, D. Y, Xu, Y Z., Chen, J. T., Wang, M. and Ge, S. Y, 1999. The effects of chronic lead exposure on long-term depression in area CA1 and dentate gyrus of rat hippocampus in vitro.Brain Res.818,153-159.
Zucker,R.S.,1989.Short-term synaptic plasticity.Annu P,ev Neurosci.12,13-31.
Zucker,R.S.,1999.Calcium- and activity-dependent synaptic plasticity.Curt Opin Neurobiol.9,305-313.
Alkondon M, Costa ACS, Radhakrishnan V, Aronstam RS, Albuquerque EX, Selective blockade of NMDA-activated channel currents may be implicated in learning deficits caused by lead. FEBS Lett (1990) 261:124-30
Altmann L, Impairment of long-term potentiation and learning following chronic lead exposure.Toxicol Lett (1993) 66:105-12
Altmann L, Impairment of long-term potentiation and learning following chronic lead exposure.Toxicol Lett (1993) 66:105-12
Altmann L, Sveinsson K, Wiegand H, Long-term potentiation in rat hippocampal slices is impaired following acute lead perfusion. Neurosci Lett (1991) 128:124-130
Ashby JAS, A neurological and biochemical study of early lead poisoning. Br J Ind (1980) 37:133-140.
Audesirk G, Electrophysiology of lead intoxication effects on voltage-sensitive ion channels.Newotoxicology (1993) 14: 137-147
Balbus-Kornfeld JM, Stewart W, Bolla KI, Schwartz BS, Cumulative exposure to inorganic lead and neurobehav ioral test performance in adults: an epidemiological review. Occup Enviro Med (1995)52:2-12
Bellinger DC, Leviton A, Waternaux C. Longitudinal analyses of prenatal and postnatal lead exposure and early cognitive development. N Engl J Med. (1987) 316:1037-43
Bellinger DC, Sloman J, Leviton A, Rabinowitz M. Low level exposure and children's cognitive function in the preschool years. Pediatrics (1991) 87: 219-227
Bellinger DC, Stilfs KM, Needleman HL, Low-level lead exposure, intelligence and academic achievement: a long-term follow-up study. Pediatrics, (1992) 90: 855-861
Bilsselberg D, Evans ML, Rahmann H, Carpenter DO, Lead and zinc block a voltage-activated calcium channel of Aplysia neurons. J. Neurophysiol. (1991) 65: 786-795.
Busselberg D, Platt B, Michael D, Carpenter DO, Mammalian voltage-activated calcium channel currents are blocked by Pb~(++)Zn~(++),and Al~(3+). J Neurophysiol (1994) 71: 234-245
Cantarow A, Trumper M, (1944) Lead poisoning. Baltimore, MD: Williams and Wilkins. Cory-Slechta D. MK-801 subsensitivity following postweaning lead exposure. Neurotoxicology (1995a) 16: 83-96
Cory-Slechta DA, Relationships between lead-induced learning impairments and changes in dopaminergic, cholinergic, and glutamatergic neurotransmitter system functions.Ann Rev Pharmacol Toxicol (1995b) 35: 391-415
Dai XQ, Ruan DY, Chen JT, Wang M, Cai L The effects of lead on transient outward currents of acutely dissociated rat dorsal root ganglion. Brain Res. (2001) 904:327-340
Davis JM, Svendsgaard DJ Nerve conduction velocity and lead: a critical review and meta-analysis. In Johnson BL (editors): Advances in Neurobehavioral Toxicology: Application in Enviromental and Occupational Health. Chelsea, Michigan: Lewis Publishers, (1990) p:353-376.
Ellen K, Silbergeld. Subcellular mechanisms of lead neurotoxicity. Brain Res (1978) 148:451-467
Feldman RG, Haddow J, Kopito L, Schwachman H, Altered peripheral nerve conduction velocity: chronic lead intoxication in children. Am JDis Child(1973) 125: 39-41.
Finkelstein Y, Mechanism of lead-induced neurotoxicity. Shaare Zedek Medical Center Fjerdingstad EJ, Hippocampus: Selective concentration of lead in the normal rat brain. Brain Res.(1974)80:350-354
Guilarte TR, Miceli RC, Age-dependent effects of lead on [3H]MK-801 binding to the NMDA receptor-gated ionophore: in vitro and in vivo studies. Neurosci Lett. (1992) 148:27-30
Haden ST, Brown EM, Stoll AL, Scott J, Fuleihan GE.The effect of lithium on calcium-induced changes in adrenocorticotrophin levels J Clin Endocrinol Metab (1999) 84:198-200
Hori N, Busselberg D. Matthew MR, Parsons PJ, Carpenter DO, Lead blocks LTP by an action not at NMDA receptors.Exp Neurol (1993) 119: 192-97
Lasley SM, Gilbert ME, Presynaptic glutamatergic function in dentate gyrus in vivo is dimished by chronic exposure to inorganic lead.Brain Res (1996) 736:125-34
Lasley SM, Polan-Curtain J, Armstrong DL, Chronic exposure to environmental levels of lead impairs in vivo induction of long-term potentiation. Brain Res (1993) 614: 347-51
Madeja M, Mubhoff U, Binding N, Witting U, Speckmann EJ, Effects of Pb~(2+) on delayed-rectifier potassium channels in acutely isolated hippocampal neurons. J. Neurophysiol.(1997)78: 2649-2654.
Markovac J, Goldstein GW, Picomolar concentrations of lead stimulate brain protein kinase C.Nature (1988)334: 71-73
Mayer ML, Westbrook GL, A voltage-clamp analysis of inward (anomalous) rectification in mouse spinal sensory ganglion neurons. J Physiol. (1983) 340: 19-45
Minnema DJ, Calcium influx and neurotransmitter release from rat hippocampal synaptosomes exposed to lead. Toxicol App Pharmacol (1988) 92: 351-57
Moriyoshi K, Masu M, Ishii T, Shigemoto R, Mizuno N, Nakanishi S, Molecular cloning and characterization of the rat NMDA receptor. Nature (1991) 354: 31-7.
Murata K, Araki S, Yokoyama K, Uchida E, Fujimura Y, Assessment of central, peripheral, and autonomic nervous system functions in lead workers: neuroelectrophysiological studies.Environ Res. (1993) 61: 323-336
Nathanson JA, Bloom FE, Lead-induced inhibition of brain adenyl cyclase. Nature (1975) 255:419-20
Needleman HL. Low-level lead exposure: the clinical implication of current research. (1989) Raven press New York
Pasternak G, Becker CE, Lash A, Bowler R, Estrin WJ, Law D, Cross-sectional neurotoxicology study of lead-exposed cohort. Clin Toxicol. (1989) 27: 37-51
Riess JA, Needleman HL, Cognitive, neural, behavioral effects of low-level lead exposure. The Vulnerable brain and environmental risks. (1992) Plenum press New York
Ruan DY, Chen JT.Zhao C. et al. Impairment of long-term potentiation and paired-pulse facilitation in rat hippocampal detate gyrus following developmental lead exposure in vivo.Brain Res (1998) 806:196-201.
Ruan DY, Yan KF, Ge SY et al. Effects of chronic lead exposure on short-term and long-term depression in area CAl of rat hippocampus in vivo. Chemosphere (2000) 41: 165-71.
Rubens O, Logina I, Kravale I, Eglite M, Donaghy M, Peripheral neuropathy in chronic occupational inorganic lead exposure: a clinical and electrophysiological study. J Newol Neurosurg Psychiatry. (2001) 71: 200-4.
Schwartz BS, Lee BK, Lee GS, Stewart WF, Lee SS, Hwang KY, Ahn KD, Kim YB, Bolla KI,Simon D, Parsons PJ, Todd AC, Associations of blood lead, dimercaptosuccinic acid-chelatable lead, and tibia lead with neurobehavioral test scores in South Korean lead workers.Am J Epidemiol. (2001) 153: 453-64.
Seppalainen AM, Hernberg S, Sensitive technique for detecting subclinical lead neuropathy. Br J Ind Med. (1972)29: 443-449
Shellenberger M, Effects of early lead exposure on neurotransmitter systems in the brain: a review with commentary. Neurotoxicol 1998,45: 117-22
Sierra EM, Rowles TK, Martin J- Bratton GR, Womac C, Low level lead neurotoxicity in a pregnant guinea pigs model: Nueroglial enzyme activities and brain trace metal concentrations Toxicology 1989, 59: 81-96
Sierra EM, Tiffany-Castiglioni E, Reduction of glutamine synthetase activity in astroglia exposed in culture to low level levels of inorganic lead.Toxicology 1991, 65: 295-304
Simons TJ Lead-calcium interactions in cellular lead toxicity. Neurotoxicology (1993) 14: 77-85.
Singer R, Valciukas JA, Lilis R, Lead exposure and nerve conduction velocity: the differential time course of sensory and motor nerve effects.Neurotoxicology(1983)4:193-202
Stoclet JC,Gerard D,Kilhoffer MC,Lugnier C,Miller R,Schaeffer P Calmodulin and its role in intracellular calcium regulation.Prog Neurobiol 1987,29:321-64
Stokes L,Letz R,Gerr F,Kolczak M,McNeill FE,Chettle DR,Kaye WE,Neurotoxicity in young adults 20 years after childhood exposure to lead:the Bunker Hill experience.Occup Environ Med.(1998)55:507-16.
Sui L,Ge SY,Ruan DY et al.Age-dependent impairment of long-term depression in area CA1and DG of rat hippocampus following developmental lead exposure in vitro.Neurotoxicol Teratol(2000)22:381-387.
Sui L,Ge SY,Ruan DY et al.Two components of long-term depression are impaired by chronic lead exposure in area CA1 and dentate gyms of rat hippocampus in vitro.Neurotoxicol Teratol (2000)2(5):741-9.
Talukder G,Harrison NL,On the mechanism of modulation of transient outward currents in cultured rat hippocampal neurons by di- and trivalent cations.J.Neurophisiol.(1995)73:73-79.
Tassler PL,Schwartz BS,Coresh J,Stewart WF,Todd AC,Associations of tibia lead,DMSA-chelatable lead,and blood lead with measures of peripheral nervous system function in former organolead manufacturing workers.American J.Ind Med.(2001)39:254-261.
Triebig G,Weltle D,Valentin H,Investigations on neurotoxicity of chemical substances at the workplace.Int Arch Occup Environ Health(1984)53:189-204.
Ujihara H,Sasa M,Ban T,Selective blockade of p-type calcium channels by lead in cultured hippocampal neurons.Jpn.J.Pharmacol.(1995)67:267-269
Wiegand H,Altmann L Neurophysiological aspects of hippocampal neurotoxicity.Neurotoxicology 1994,15:451-8
Xu YZ,Ruan DY,Wu Yet al.Nitric Oxide affects LTP in Area CA1 and CA3 of hippocampus in low-level lead exposed rat.Neurotoxicol Teratol(1998)20(1):69-73.
Yeh J,Chang Y,Wang J,Combined electroneurographic and electromyographic studies in lead workers.Occup Environ Med(1995)52:415-419.
Zimmerman-Tansella C,Campara P,D'Andrea F,Savonitto C,Tansella M,Psychological and physical complaints of subjects with low exposure to lead.Hum Toxicol.(1983)2:615-623.
何稼敏,铅的神经毒性作用机制。铅污染的危害与防治,P 184-7,香港新闻出版社(1997)。
陆巍,铅的神经毒作用机制。铅污染的危害与防治,P 40-42,香港新闻出版社(1997)。
阮迪云,陈聚涛,赵望发,柳素铃,顾炜玮,铅对海马齿状回L-LTP和双脉冲发应的影响.广东微量元素科学(1998)5:25-29
Abe K, Nakata A, Mizutani A, Saito H. 1994. Facilitatory but nonessential role of the muscarinic cholinergic system in the generation of long-term potentiation of population spikes in the dentate gyrus in vivo. Neuropharmacology 33(7):847-52.
Auerbach JM, Segal M. 1996. Muscarinic receptors mediating depression and long-term potentiation in rat hippocampus. J Physiol 492 (Pt 2):479-93.
Aura J, Sirvio J, Riekkinen P. 1997. Methoctramine moderately improves memory but pirenzepine disrupts performance in delayed non-matching to position test. European Journal of Pharmacology 333(2-3): 129-134.
Bartus RT, Dean RL, 3rd B, B., Lippa AS. 1982. The cholinergic hypothesis of geriatric memory dysfunction. Science 217:408-414.
Berkeley JL, Gomeza J, Wess J, Hamilton SE, Nathanson NM, Levey AI. 2001. M-l muscarinic acetylcholine receptors activate extracellular signal-regulated kinase in CA1 pyramidal neurons in mouse hippocampal slices. Molecular and Cellular Neuroscience 18(5):512-524.
Bliss TVP, Collingridge GL. 1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
Blitzer RD, Gil O, Landau EM. 1990. Cholinergic stimulation enhances long-term potentiation in the CA1 region of rat hippocampus. Neurosci Lett 119(2):207-10.
Boddeke EW, Enz A, Shapiro G. 1992. SDZ ENS 163, a selective muscarinic Ml receptor agonist, facilitates the induction of long-term potentiation in rat hippocampal slices. Eur J Pharmacol 222(1):21-5.
Burgard EC, Sarvey JM. 1990. Muscarinic receptor activation facilitates the induction of long-term potentiation (LTP) in the rat dentate gyrus. Neurosci Lett 116(l-2):34-9.
Coyle JT, Price DL, DeLong MR. 1983. Alzheimer's disease: a disorder of cortical cholinergic innervation. Science 219(4589): 1184-90.
Hajos N, Papp EC, Acsady L, Levey AI, Freund TF. 1998. Distinct interneuron types express m2 muscarinic receptor immunoreactivity on their dendrites or axon terminals in the hippocampus. Neuroscience 82(2):355-76.
Hamilton SE, Nathanson NM. 2001. The Ml receptor is required for muscarinic activation of mitogen-activated protein (MAP) kinase in murine cerebral cortical neurons. J Biol Chem 276(19):15850-3.
Harvey J, Balasubramaniam R, Collingridge GL. 1993. Carbachol can potentiate N-methyl-d-aspartate responses in the rat hippocampus by a staurosporine and thapsigargin-insensitive mechanism. Neurosci. Lett 162:165-168.
Hori H, Haruta K, Nanki M, Sakamoto N, Uemura K, Matsubara T, Itoh K, Iguchi A. 1995.Pressor-Response Induced by the Hippocampal Administration of Neostigmine Is Suppressed by Ml Muscarinic Antagonist. Life Sciences 57(20): 1853-1859.
Inglis FM, Fibiger HC. 1995. Increases in hippocampal and frontal cortical acetylcholine release associated with presentation of sensory stimuli. Neuroscience 66(1 ):81 -6.
Jacob SN. Choe C-U, Uhlen P, Degray B, Yeckel MF, Ehrlich BE. 2005. Signaling microdomains regulate inositol 1,4,5-trisphosphate-mediated intracellular calcium transients in cultured neurons. The Journal of Neuroscience 25:2853-2864.
Jerusalinsky D, Kornisiuk E, Izquierdo I. 1997. Cholinergic neurotransmission and synaptic plasticity concerning memory processing. Neurochem. Res 22:507-515.
Levey AI. 1996. Muscarinic acetycholine receptor expression in memory circuits: implications for treatment of Alzheimer disease. Proc.Natl.Acad.sci.USA 93:13541-13546.
Levey AI, Edmunds SM, Koliatsos VK, Wiley RG, Heilman CJ. 1995. Expression of m1-m4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulation by cholinergic innervation. The Journal of Neuroscience 15:4077-4092.
Levey AI, Kitt C A. Simonds WF, Price DL, Brann MR. 1991. Identification and localization of muscarinic acetylcholine receptor protein in brain with subtype-specific antibodies. J.Neurosci 11:3218-3226.
Li S, Cullen WK, Anwyl R, Rowan MJ. 2007. Muscarinic acetylcholine receptor-dependent induction of persistent synaptic enhancement in rat hippocampus in vivo. Neuroscience 144(2):754-61.
Madison DV, Lancaster B, Nicoll RA. 1987. Voltage clamp analysis of cholinergic action in the hippocampus. J. Neurosci 7:733-741.
Mastropaolo J, Nadi NS, Ostrowski NL, Crawley JN. 1988. Galanin antagonizes acetylcholine on a memory task in basal forebrain-lesioned rats. Proc Natl Acad Sci U S A 85(24):9841-5.
Messer WS, Bohnett M, Stibbe J. 1990. Evidence for a Preferential Involvement of Ml Muscarinic Receptors in Representational Memory. Neuroscience Letters 116(1-2):184-189.
Mesulam MM, Mufson EJ, Wainer BH, Levey AI. 1983. Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Chl-Ch6). Neuroscience 10:1185-1201.
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(5):1267-75.
Patil MM, Linster C, Lubenov E, Hasselmo ME. 1998. Cholinergic agonist carbachol enables associative long-term potentiation in piriform cortex slices. J Neurophysiol 80(5):2467-74.
Rouse ST, Edmunds SM, Yi H, Gilmor ML, Levey AI. 2000. Localization of M(2) muscarinic acetylcholine receptor protein in cholinergic and non-cholinergic terminals in rat hippocampus. Neurosci Lett 284(3): 182-6.
Saito K, Yoshioka M, Kohya T, Kitabatake A. 1994. Involvement of Muscarinic Ml Receptor in the Central Pathway of the Serotonin-Induced Bezold-Jarisch Reflex in Rats. Journal of the Autonomic Nervous System 49(l):61-68.
Segal M, Auerbach JM. 1997. Muscarinic receptors involved in hippocampal plasticity. Life Sci.60:1085-1091.
Shimoshige Y, Maeda T, Kaneko S, Akaike A, Satoh M. 1997. Involvement of M2 receptor in an enhancement of long-term potentiation by carbachol in Schaffer collateral-CAl synapses of hippocampal slices. Neuroscience Research 27:175-180.
Shinoe T, Matsui M, Taketo MM, Manabe T. 2005. Modulation of synaptic plasticity by physiological activation of Ml muscarinic acetylcholine receptors in the mouse hippocampus. J Neurosci 25(48): 11194-200.
Winkler J, Thal LJ, Gage FH, Fisher LJ. 1998. Cholinergic strategies for Alzheimer's disease. J Mol Med 76(8):555-67.
Adhami, V. M., Husain, R., Agarwal, A. K. and Seth, P. K., 2000. Intrahippocampal cholinergic-rich transplants restore lead-induced deficits: a preliminary study in rats.Neurotoxicol Teratol. 22,41-53.
Aigner, T. G, 1995. Pharmacology of memory: cholinergic-glutamatergic interactions. Curr Opin Neurobiol.5,155-160.
Alkondon, M., Costa, A. C, Radhakrishnan, V., Aronstam, R. S. and Albuquerque, E. X., 1990.Selective blockade of NMDA-activated channel currents may be implicated in learning deficits caused by lead. FEBS Lett. 261, 124-130.
Alkondon, M., Pereira, E. F., Barbosa, C. T. and Albuquerque, E. X., 1997. Neuronal nicotinic acetylcholine receptor activation modulates gamma-aminobutyric acid release from CAI neurons of rat hippocampal slices. J Pharmacol Exp Ther. 283,1396-1411.
Auerbach, J. M. and Segal, M., 1994. A novel cholinergic induction of long-term potentiation in rat hippocampus. J Neurophysiol. 72, 2034-2040.
Auerbach, J. M. and Segal, M., 1996. Muscarinic receptors mediating depression and long-term potentiation in rat hippocampus. J Physiol. 492 (Pt 2), 479-493.
Bartus, R. T., Dean, R. L., 3rd, Beer, B. and Lippa, A. S., 1982. The cholinergic hypothesis of geriatric memory dysfunction. Science. 217, 408-414.
Benardo, L. S. and Prince, D. A., 1982. Cholinergic excitation of mammalian hippocampal pyramidal cells. Brain Res. 249, 315-331.
Blitzer, R. D., Gil, O. and Landau, E. M., 1990. Cholinergic stimulation enhances long-term potentiation in the CAI region of rat hippocampus. Neurosci Lett. 119,207-210.
Braga, M. F., Pereira, E. F. and Albuquerque, E. X., 1999. Nanomolar concentrations of lead inhibit glutamatergic and GABAergic transmission in hippocampal neurons. Brain Res. 826,22-34.
Buckley, N. J., Bonner, T. I. and Brann, M. R., 1988. Localization of a family of muscarinic receptor mRNAs in rat brain. J Neurosci. 8, 4646-4652.
Busselberg, D., Evans, M. L., Rahmann, H. and Carpenter, D. O., 1991. Lead and zinc block a voltage-activated calcium channel of Aplysia neurons. J Neurophysiol. 65, 786-795.
Conn, J. and Cory-Slechta, D. A., 1993. Subsensitivity of lead-exposed rats to the accuracy-impairing and rate-altering effects of MK-801 on a multiple schedule of repeated learning and performance. Brain Res. 600,208-218.
Cory-Slechta, D. A. and Pokora, M. J., 1995. Lead-induced changes in muscarinic cholinergic sensitivity. Neurotoxicology. 16, 337-347.
Coyle, J. T., Price, D. L. and DeLong, M. R., 1983. Alzheimer's disease: a disorder of cortical cholinergic innervation. Science. 219,1184-1190.
de Sevilla, D. F., Cabezas, C, de Prada, A. N., Sanchez-Jimenez, A. and Buno, W., 2002. Selective muscarinic regulation of functional glutamatergic Schaffer collateral synapses in rat CAl pyramidal neurons. J Physiol. 545, 51-63.
Dudar, J. D., 1977. The role of the septal nuclei in the release of acetyl-choline from the rabbit cerebral cortex and dorsal hippocampus and the effect of atropine. Brain Res. 129,237-246.
Frotscher, M. and Leranth, C, 1985. 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.
Frotscher, M., Vida, I. and Bender, R., 2000. Evidence for the existence of non-GABAergic,cholinergic interneurons in the rodent hippocampus. Neuroscience. 96,27-31.
Gaztelu, J. M. and Buno, W., Jr., 1982. Septo-hippocampal relationships during EEG theta rhythm. Electroencephalogr Clin Neurophysiol. 54,375-387.
Goda, Y. and Stevens, C. F., 1996. Synoptic plasticity: the basis of particular types of learning.CurrBiol.6, 375-378.
Hamill, O. P., Marty, A., Neher, E., Sakmann, B. and Sigworth, F. J., 1981. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches.Pflugers Arch.391,85-100.
Harvey, J., Balasubramaniam, R. and Collingridge, G. L., 1993. Carbachol can potentiate N-methyl-D-aspartate responses in the rat hippocampus by a staurosporine and thapsigargin-insensitive mechanism. Neurosci Lett. 162, 165-168.
Hasselmo, M. E., 1999. Neuromodulation: acetylcholine and memory consolidation. Trends Cogn Sci.3, 351-359.
Hefft, S., Hulo, S., Bertrand, D. and Muller, D., 1999. Synaptic transmission at nicotinic acetylcholine receptors in rat hippocampal organotypic cultures and slices. J Physiol. 515 ( Pt 3), 769-776.
Hersch, S. M., Gutekunst, C. A., Rees, H. D., Heilman, C. J. and Levey, A. I., 1994. Distribution of m1-m4 muscarinic receptor proteins in the rat striatum: light and electron microscopic immunocytochemistry using subtype-specific antibodies. J Neurosci. 14,3351-3363.
Hersch, S. M. and Levey, A. I., 1995. Diverse pre- and post-synaptic expression of m1-m4 muscarinic receptor proteins in neurons and afferents in the rat neostriatum. Life Sci. 56,931-938.
Hounsgaard, J., 1978. Presynaptic inhibitory action of acetylcholine in area CAI of the hippocampus. Exp Neurol. 62, 787-797.
Huerta, P. T. and Lisman, J. E., 1995. Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CAI in vitro. Neuron. 15, 1053-1063.
Hwang, T. N. and Copenhagen, D. R., 1999. Automatic detection, characterization, and discrimination of kinetically distinct spontaneous synaptic events. J Neurosci Methods. 92,65-73.
Iga, Y., Arisawa, H., Ise, M., Yasuda, H. and Takeshita, Y., 1996. Modulation of rhythmical slow activity, long-term potentiation and memory by muscarinic receptor agonists. Eur J Pharmacol.308,13-19.
Jett, D. A. and Guilarte, T. R., 1995. Developmental lead exposure alters N-methyl-D-aspartate and muscarinic cholinergic receptors in the rat hippocampus: an autoradiographic study.Neurotoxicology. 16, 7-18.
Lewis, P. R. and Shute, C. C, 1967. The cholinergic limbic system: projections to hippocampal formation, medial cortex, nuclei of the ascending cholinergic reticular system, and the subfornical organ and supra-optic crest. Brain. 90, 521-540.
Macadar, O., Roig, J. A., Monti, J. M. and Budelli, R., 1970. The functional relationship between septal and hippocampal unit activity and hippocampal theta rhythm. Physiol Behav. 5,1443-1449.
Madison, D. V., Lancaster, B. and Nicoll, R. A., 1987. Voltage clamp analysis of cholinergic action in the hippocampus. J Neurosci. 7, 733-741.
Madison, D. V, Malenka, R. C. and Nicoll, R. A., 1991. Mechanisms underlying long-term potentiation of synaptic transmission. Annu Rev Neurosci. 14, 379-397.
Marino, M. J., Rouse, S. T., Levey, A. I., Potter, L. T. and Conn, P. J., 1998. Activation of the genetically defined ml muscarinic receptor potentiates N-methyl-D-aspartate (NMDA) receptor currents in hippocampal pyramidal cells. Proc Natl Acad Sci U S A. 95,11465-11470.
Mazzolini, M., Traverso, S. and Marchetti, C, 2001. Multiple pathways of Pb(2+) permeation in rat cerebellar granule neurones. J Neurochem. 79, 407-416.
Minnema, D. J., Michaelson, I. A. and Cooper, G. P., 1988. Calcium efflux and neurotransmitter release from rat hippocampal synaptosomes exposed to lead. Toxicol Appl Pharmacol. 92,351-357.
Patil, M. M, Linster, C, Lubenov, E. and Hasselmo, M. E., 1998. Cholinergic agonist carbachol enables associative long-term potentiation in piriform cortex slices. J Neurophysiol. 80,2467-2474.
Qian, J. and Saggau, P., 1997. Presynaptic inhibition of synaptic transmission in the rat hippocampus by activation of muscarinic receptors: involvement of presynaptic calcium influx.Br J Pharmacol. 122,511-519.
Richter, M., Schilling, T. and Muller, W., 1999. Muscarinic control of intracortical connections to layer II in rat entorhinal cortex slice. Neurosci Lett. 273, 200-202.
Ruan, D. Y., Chen, J. T., Zhao, C, Xu, Y. Z., Wang, M. and Zhao, W. F., 1998. Impairment of long-term potentiation and paired-pulse facilitation in rat hippocampal dentate gyrus following developmental lead exposure in vivo. Brain Res. 806,196-201.
Ruan, D. Y, Yan, K. F., Ge, S. Y., Xu, Y. Z., Chen, J. T. and Wang, M., 2000. Effects of chronic lead exposure on short-term and long-term depression in area CAl of the rat hippocampus in vivo. Chemosphere. 41,165-171.
Silbergeld, E. K. and Adler, H. S., 1978. Subcellular mechanisms of lead neurotoxicity. Brain Res.148,451-467.
Toth, K. and McBain, C. J., 2000. Target-specific expression of pre- and postsynaptic mechanisms.J Physiol. 525 Pt1,41-51.
Uteshev, V, Busselberg, D. and Haas, H. L., 1993. Pb2+ modulates the NMDA-receptor-channel complex. Naunyn Schmiedebergs Arch Pharmacol. 347,209-213.
Valentino, R. J. and Dingledine, R., 1981. Presynaptic inhibitory effect of acetylcholine in the hippocampus. J Neurosci. 1, 784-792.
Van der Kloot, W, 1989. Statistical and graphical methods for testing the hypothesis that quanta are made up of subunits. J Neurosci Methods. 27, 81-89.
Wei, J., Walton, E. A., Milici, A. and Buccafusco, J. J., 1994. m1-m5 muscarinic receptor distribution in rat CNS by RT-PCR and HPLC. J Neurochem. 63,815-821.
Winkler, J., Thal, L. J., Gage, F. H. and Fisher, L. J., 1998. Cholinergic strategies for Alzheimer's disease. J Mol Med. 76, 555-567.
Xu, Y. Z., Ruan, D. Y., Wu, Y, Jiang, Y. B., Chen, S. Y, Chen, J. and Shi, P., 1998. Nitric oxide affects LTP in area CAl and CA3 of hippocampus in low-level lead-exposed rat. Neurotoxicol Teratol. 20,69-73.
Yun, S. H., Cheong, M. Y, Mook-Jung, I., Huh, K., Lee, C. and Jung, M. W., 2000. Cholinergic modulation of synaptic transmission and plasticity in entorhinal cortex and hippocampus of the rat. Neuroscience. 97, 671-676.
Zhang, L. and Warren, R. A., 2002. Muscarinic and nicotinic presynaptic modulation of EPSCs in the nucleus accumbens during postnatal development. J Neurophysiol. 88, 3315-3330.
Zhao, W. F., Ruan, D. Y, Xu, Y. Z., Chen, J. T., Wang, M. and Ge, S. Y, 1999. The effects of chronic lead exposure on long-term depression in area CAl and dentate gyrus of rat hippocampus in vitro. Brain Res. 818,153-159.
Zucker, R. S., 1989. Short-term synaptic plasticity. Annu Rev Neurosci. 12,13-31.
Zucker, R. S., 1999. Calcium- and activity-dependent synaptic plasticity. Curr Opin Neurobiol. 9,305-313.