Nicotinic acetylcholine receptors at glutamate synapses facilitate long-term depression or potentiation

Journal of Neuroscience

Volumn 25, Issue 26, 2005, Pages 6084-6091

  Ge, Shaoyu ^a   Dani, John A ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Cholinergic; Hippocampus; Nicotine addiction; Nicotinic receptors; Synaptic modulation; Synaptic plasticity

Indexed keywords

NICOTINIC RECEPTOR;

ACTION POTENTIAL; ADDICTION; ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; ATTENTION; CONTROLLED STUDY; ELECTROSTIMULATION; GRANULE CELL; HIPPOCAMPUS; INTERNEURON; LEARNING; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MEMORY; MOUSE; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PARASYMPATHETIC INNERVATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SYNAPSE;

ACETYLCHOLINE; ANIMALS; DENDRITES; ELECTRIC STIMULATION; GLUTAMIC ACID; HIPPOCAMPUS; LONG-TERM DEPRESSION (PHYSIOLOGY); LONG-TERM POTENTIATION; MICE; MICE, INBRED C57BL; PYRAMIDAL CELLS; RECEPTORS, NICOTINIC; SYNAPSES;

EID: 21544450517     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0542-05.2005     Document Type: Article

References (67)

1. Albuquerque EX, Alkondon M, Pereira EF, Castro NG, Schrattenholz A, Barbosa CT, Bonfante-Cabarcas R, Aracava Y, Eisenberg HM, Maelicke A (1997) Properties of neuronal nicotinic acetylcholine receptors: pharmacological characterization and modulation of synaptic function. J Pharmacol Exp Ther 280:1117-1136.
2. Alkondon M, Albuquerque EX (1993) Diversity of nicotinic acetylcholine receptors in rat hippocampal neurons. I. Pharmacological and functional evidence for distinct structural subtypes. J Pharmacol Exp Ther 265:1455-1473.
3. Alkondon M, Albuquerque EX (2001) Nicotinic acetylcholine receptor alpha7 and alpha4beta2 subtypes differentially control GABAergic input to CA1 neurons in rat hippocampus. J Neurophysiol 86:3043-3055.
4. Alkondon M, Rocham ES, Maelicke A, Albuquerque EX (1996) Diversity of nicotinic acetylcholine receptors in rat brain. V. Alpha-bungarotoxin-sensitive nicotinic receptors in olfactory bulb neurons and presynaptic modulation of glutamate release. J Pharmacol Exp Ther 278:1460-1471.
5. Alkondon M, Pereira EF, Barbosa CTF, Albuquerque EX (1997) Neuronal nicotinic acetylcholine receptor activation modulates gamma-aminobutyric acid release from CA1 neurons of rat hippocampal slices. J Pharmacol Exp Ther 283:1396-1411.
6. Alkondon M, Pereira EF, Albuquerque EX (1998) Alpha-bungarotoxin- and methyllycaconitine-sensitive nicotinic receptors mediate fast synaptic transmission in interneurons of rat hippocampal slices. Brain Res 810:257-263.
7. Alkondon M, Pereira EF, Eisenberg HM, Albuquerque EX (2000) Nicotinic receptor activation in human cerebral cortical interneurons: a mechanism for inhibition and disinhibition of neuronal networks. J Neurosci 20:66-75.
8. Aramakis VB, Metherate R (1998) Nicotine selectively enhances NMDA receptor-mediated synaptic transmission during postnatal development in sensory neocortex. J Neurosci 18:8485-8495.
9. Bancroft A, Levin ED (2000) Ventral hippocampal alpha4beta2 nicotinic receptors and chronic nicotine effects on memory. Neuropharmacology 39:2770-2778.
10. Berg DK, Conroy WG (2002) Nicotinic alpha 7 receptors: synaptic options and downstream signaling in neurons. J Neurobiol 53:512-523.
11. Bi GQ, Poo MM (1998) Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18:10464-10472.
12. Castro NG, Albuquerque EX (1995) Alpha-bungarotoxin-sensitive hippocampal nicotinic receptor channel has a high calcium permeability. Biophys J 68:516-524.
13. Deisseroth K, Bito H, Tsien RW (1996) Signaling from synapse to nucleus: postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron 16:89-101.
14. Frazier CJ, Rollins YD, Breese CR, Leonard S, Freedman R, Dunwiddie TV (1998) Acetylcholin activate an α-bungarotoxin-sensitive nicotinic current in rat hippocampal interneurons but not pyramidal cells. J Neurosci 18:1187-1195.
15. Froemke RC, Poo MM, Dan Y (2005) Spike-timing-dependent synaptic plasticity depends on dendritic location. Nature 434:221-225.
16. Fujii S, Ji Z, Morita N, Sumikawa K (1999) Acute and chronic nicotine exposure differentially facilitate the induction of LTP. Brain Res 846:137-143.
17. Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA (1996) Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 83:713-716.
18. Grigoryan GA, Mitchell SN, Hodges H, Sinden JD, Gray JA (1994) Are the cognitive-enhancing effects of nicotine in the rat with lesions to the forebrain cholinergic projection system mediated by an interaction with the noradrenergic system? Pharmacol Biochem Behav 49:511-521.
19. Hamid S, Dawe GS, Grav JA, Stephenson JD (1997) Nicotine induces long-lasting potentiation in the dentate gyrus of nicotine-primed rats. Neurosci Res 29:81-85.
20. Hefft S, Hulo S, Bertrand D, Muller D (1999) Synaptic transmission at nicotinic acetylcholine receptors in rat hippocampal organotypic cultures and slices. J Physiol (Lond) 515:769-776.
21. Helmchen F, Borst JG, Sakmann B (1997) Calcium dynamics associated with a single action potential in a CNS presynaptic terminal. Biophys J 72:1458-1471.
22. Ji D, Dani JA (2000) Inhibition and disinhibition of pyramidal neurons by activation of nicotinic receptors on hippocampal interneurons. J Neurophysiol 83:2682-2690.
23. Ji D, Lape R, Dani JA (2001) Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity. Neuron 31:131-141.
24. Jones S, Yakel JL (1997) Functional nicotinic ACh receptors on interneurons in the rat hippocampus. J Physiol (Lond) 504:603-610.
25. Jones S, Sudweeks S, Yakel JL (1999) Nicotinic receptors in the brain: correlating physiology with function. Trends Neurosci 22:555-561.
26. 2+ regulation of nicotinic acetylcholine receptor channels in rat hippocampal CA1 neurons. J Neurosci 23:9024-9031.
27. Levin ED, Rezvani AH (2000) Development of nicotinic drug therapy for cognitive disorders. Eur J Pharmacol 393:141-146.
28. Levin ED, Simon BB (1998) Nicotinic acetylcholine involvement in cognitive function in animals. Psychopharmacology 138:217-230.
29. Levin ED, Christopher NC, Briggs SJ, Rose JE (1993) Chronic nicotine reverses working memory deficits caused by lesions of the fimbria or medial basalocortical projection. Brain Res Cogn Brain Res 1:137-143.
30. Levin ED, Conners CK, Silva D, Hinton SC, Meek WH, March J, Rose JE (1998) Transdermal nicotine effects on attention. Psychopharmacology 140:135-141.
31. Li C, Lu J, Wu C, Duan S, Poo M (2004) Bidirectional modification of presynaptic neuronal excitability accompanying spike timing-dependent synaptic plasticity. Neuron 41:257-268.
32. Maelicke A, Samochocki M, Jostock R, Fehrenbacher A, Ludwig J, Albuquerque EX, Zerlin M (2001) Allosteric sensitization of nicotinic receptors by galantamine, a new treatment strategy for Alzheimer's disease. Biol Psychiatry 49:279-288.
33. Maggi L, Le Magueresse C, Changeux JP, Cherubini E (2003) Nicotine activates immature "silent" connections in the developing hippocampus. Proc Natl Acad Sci USA 100:2059-2064.
34. Maggi L, Sola E, Minneci F, Le Magueresse C, Changeux JP, Cherubini E (2004) Persistent decrease in synaptic efficacy induced by nicotine at Schaffer collateral-CA1 synapses in the immature rat hippocampus. J Physiol (Lond) 559:863-874.
35. Malenka RC, Nicoll RA (1999) Long-term potentiation: a decade of progress? Science 285:1870-1874.
36. Malenka RC, Lancaster B, Zucker RS (1992) Temporal limits on the rise in postsynaptic calcium required for the induction of long-term potentiation. Neuron 9:121-128.
37. Mansvelder HD, McGehee DS (2000) Long-term potentiation of excitatory inputs to brain reward areas by nicotine. Neuron 27:349-357.
38. Mansvelder HD, Keath JR, McGehee DS (2002) Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas. Neuron 33:905-919.
39. Markram H, Lubke J, Frotscher M, Sakmann B (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275:213-215.
40. Martin SJ, Grimwood PD, Morris RG (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649-711.
41. McGehee DS, Role LW (1995) Physiological diversity of nicotinic acetylcholine receptors expressed by vertebrate neurons. Annu Rev Physiol 57:521-546.
42. McGehee DS, Heath MJ, Gelber S, Devay P, Role LW (1995) Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 269:1692-1696.
43. McQuiston AR, Madison DV (1999) Nicotinic receptor activation excites distinct subtypes of interneurons in the rat hippocampus. J Neurosci 19:2887-2896.
44. Newhouse PA, Potter A, Levin ED (1997) Nicotinic system involvement in Alzheimer's and Parkinson's diseases. Implications for therapeutics. Drugs Aging 11:206-228.
45. Ohno M, Yamamoto T, Watanabe S (1993) Blockade of hippocampal nicotinic receptors impairs working memory but not reference memory in rats. Pharmacol Biochem Behav 45:89-93.
46. Paterson D, Nordberg A (2000) Neuronal nicotinic receptors in the human brain. Prog Neurobiol 61:75-111.
47. Perry E, Martin-Ruiz C, Lee M, Griffiths M, Johnson M, Piggott M, Haroutunian V, Buxbaum JD, Nasland J, Davis K, Gotti C, Clementi F, Tzartos S, Cohen O, Soreq H, Jaros E, Perry R, Ballard C, McKeith I, Court J (2000) Nicotinic receptor subtypes in human brain aging, Alzheimer and Lewy body diseases. Eur J Pharmacol 393:215-222.
48. Picciotto MR, Zoli M, Lena C, Bessis A, Lallemand Y, Le Novere N, Vincent P, Pich EM, Brulet P, Changeux JP (1995) Abnormal avoidance learning in mice lacking functional high-affinity nicotine receptor in the brain. Nature 374:65-67.
49. Pidoplichko VI, Noguchi J, Areola OO, Liang Y, Peterson J, Zhang T, Dani JA (2004) Nicotinic cholinergic synaptic mechanisms in the ventral tegmental area contribute to nicotine addiction. Learn Mem 11:60-69.
50. Potter AS, Newhouse PA (2004) Effects of acute nicotine administration on behavioral inhibition in adolescents with attention-deficit/hyperactivity disorder. Psychopharmacology 176:182-194.
51. Radcliffe K, Dani JA (1998) Nicotinic stimulation produces multiple forms of glutamatergic synaptic enhancement. J Neurosci 18:7075-7083.
52. Rathouz MM, Vijayaraghavan S, Berg DK (1996) Elevation of intracellular calcium levels in neurons by nicotinic acetylcholine receptors. Mol Neurobiol 12:117-131.
53. Regehr WG, Delaney KR, Tank DW (1994) The role of presynaptic calcium in short-term enhancement at the hippocampal mossy fiber synapse. J Neurosci 14:523-537.
54. Role LW, Berg DK (1996) Nicotinic receptors in the development and modulation of CNS synapses. Neuron 16:1077-1085.
55. Séguéla P, Wadiche J, Dineley-Miller K, Dani JA, Patrick JW (1993) Molecular cloning, functional properties, and distribution of rat brain α7: a nicotinic cation channel highly permeable to calcium. J Neurosci 13:596-604.
56. Shao Z, Yakel JL (2000) Single channel properties of neuronal nicotinic ACh receptors in stratum radiatum interneurons of rat hippocampal slices. J Physiol (Lond) 527:507-513.
57. Sharma G, Vijayaraghavan S (2001) Nicotinic cholinergic signaling in hippocampal astrocytes involves calcium-induced calcium release from intracellular stores. Proc Natl Acad Sci USA 98:4148-4153.
58. Shoop RD, Chang KT, Ellisman MH, Berg DK (2001) Synaptically driven calcium transients via nicotinic receptors on somatic spines. J Neurosci 21:771-781.
59. A receptor-mediated postsynaptic conductance. J Neurophysiol 68:197-212.
60. Sudweeks SN, Yakel JL (2000) Functional and molecular characterization of neuronal nicotinic ACh receptors in rat CA1 hippocampal neurons. J Physiol (Lond) 527:515-528.
61. Umbriaco D, Garcia S, Beaulieu C, Descarries L (1995) Relational features of acetylcholine, noradrenaline, serotonin and GABA axon terminals in the stratum radiatum of adult rat hippocampus (CA1). Hippocampus 5:605-620.
62. Vernino S, Amador M, Luetje CW, Patrick J, Dani JA (1992) Calcium modulation and high calcium permeability of neuronal nicotinic acetylcholine receptors. Neuron 8:127-134.
63. Wada E, Wada K, Boulter J, Deneris E, Heinemann S, Patrick J, Swanson LW (1989) Distribution of α2, α3, α4 and β2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: a hybridization histochemical study in the rat. J Comp Neurol 284:314-335.
64. White HK, Levin ED (1999) Chronic four week nicotine skin patch treatment effects on cognitive performance in Alzheimer's disease. Psychopharmacology 143:158-165.
65. Wonnacott S (1997) Presynaptic nicotinic ACh receptors. Trends Neurosci 20:92-98.
66. Woolf NJ (1991) Cholinergic systems in mammalian brain and spinal cord. Prog Neurobiol 37:475-524.
67. Zhang LI, Tao HW, Holt CE, Harris WA, Poo M-m (1998) Memory from the dynamics of intrinsic membrane currents. A critical window for cooperation and competition among developing retinotectal synapses. Nature 395:37-44.