Nicotine exposure in vivo induces long-lasting enhancement of NMDA receptor-mediated currents in the hippocampus

European Journal of Neuroscience

Volumn 23, Issue 7, 2006, Pages 1819-1828

  Yamazaki, Yoshihiko ^a   Jia, Yousheng ^a   Niu, Rong ^a   Sumikawa, Katumi ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Hippocampal CA1 region; Long term potentiation; Nicotinic acetylcholine receptors; NR2B containing NMDA receptors; Rat

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; NICOTINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL MEMBRANE POTENTIAL; CIGARETTE SMOKING; CONTROLLED STUDY; DRUG DEPENDENCE; HIPPOCAMPUS; LEARNING; LONG TERM EXPOSURE; LONG TERM POTENTIATION; MEMORY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RAT; RECEPTOR INTRINSIC ACTIVITY; SYNAPSE;

ANIMALS; HIPPOCAMPUS; LONG-TERM DEPRESSION (PHYSIOLOGY); LONG-TERM POTENTIATION; NICOTINE; NICOTINIC AGONISTS; PATCH-CLAMP TECHNIQUES; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PYRAMIDAL CELLS; RATS; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; TYROSINE;

EID: 33645453172     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2006.04714.x     Document Type: Article

References (59)

1. Abdulla F.A. Bradbury E. Calaminici M.R. Lippiello P.M. Wonnacott S. Gray J.A. Sinden J.D. 1996 Relationship between up-regulation of nicotine binding sites in rat brain and delayed cognitive enhancement observed after chronic or acute nicotinic receptor stimulation. Psychopharmacology 124 323 331.
2. Abel T. Nguyen P.V. Barad M. Deuel T.A. Kandel E.R. Bourtchouladze R. 1997 Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88 615 626.
3. Alkondon M. Albuquerque E.X. 2001 Nicotinic acetylcholine receptor alpha7 and alpha4beta2 subtypes differentially control GABAergic input to CA1 neurons in rat hippocampus. J. Neurophysiol. 86 3043 3055.
4. Barria A. Malinow R. 2002 Subunit-specific NMDA receptor trafficking to synapses. Neuron 35 345 353.
5. Barria A. Malinow R. 2005 NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 48 289 301.
6. Berberich S. Punnakkal P. Jensen V. Pawlak V. Seeburg P.H. Hvalby O. Kohr G. 2005 Lack of NMDA receptor subtype selectivity for hippocampal long-term potentiation. J. Neurosci. 25 6907 6910.
7. Borgland S.L. Malenka R.C. Bonci A. 2004 Acute and chronic cocaine-induced potentiation of synaptic strength in the ventral tegmental area: electrophysiological and behavioral correlates in individual rats. J. Neurosci. 24 7482 7490.
8. Brudzynski S.M. Gibson C.J. 1997 Release of dopamine in the nucleus accumbens caused by stimulation of the subiculum in freely moving rats. Brain Res. Bull. 42 303 308.
9. 2+ stores. J. Neurochem. 81 606 614.
10. Faleiro L.J. Jones S. Kauer J.A. 2004 Rapid synaptic plasticity of glutamatergic synapses on dopamine neurons in the ventral tegmental area in response to acute amphetamine injection. Neuropsychopharmacology 29 2115 2125.
11. Frazier C.J. Rollins Y.D. Breese C.R. Leonard S. Freedman R. Dunwiddie T.V. 1998 Acetylcholine activates an α-bungarotoxin-sensitive nicotinic current in rat hippocampal interneurons, but not pyramidal cells. J. Neurosci. 18 1187 1195.
12. Fuchs R.A. Evans K.A. Ledford C.C. Parker M.P. Case J.M. Mehta R.H. See R.E. 2005 The role of the dorsomedial prefrontal cortex, basolateral amygdala, and dorsal hippocampus in contextual reinstatement of cocaine seeking in rats. Neuropsychopharmacology 30 296 309.
13. 2+ permeability of nicotinic acetylcholine receptors. Cell Calcium 35 1 8.
14. 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.
15. 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.
16. Huang Y. Lu W. Ali D.W. Pelkey K.A. Pitcher G.M. Lu Y.M. Aoto H. Roder J.C. Sasaki T. Salter M.W. MacDonald J.F. 2001 CAKβ/Pyk2 kinase is a signaling link for induction of long-term potentiation in CA1 hippocampus. Neuron 29 485 496.
17. Hyman S.E. Malenka R.C. 2001 Addiction and the brain: the neurobiology of compulsion and its persistence. Nat. Rev. Neurosci. 2 695 703.
18. Iwasaki Y. Gay B. Wada K. Koizumi S. 1998 Association of the Src family tyrosine kinase Fyn with TrkB. J. Neurochem. 71 106 111.
19. Ji D. Lape R. Dani J.A. 2001 Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity. Neuron 31 131 141.
20. Jones G.M.M. Sahakian B.J. Levy R. Warburton D.M. Gray J.A. 1992 Effects of acute subcutaneous nicotine on attention, information processing and short-term memory in Alzheimer's disease. Psychopharmacology 108 485 494.
21. Jones S. Yakel J.L. 1997 Functional nicotinic ACh receptors on interneurons in the rat hippocampus. J. Physiol. (Lond.) 504 603 610.
22. Kelley A.E. 2004 Memory and addiction: shared neural circuitry and molecular mechanisms. Neuron 44 161 179.
23. Kelley A.E. Domesick V.B. 1982 The distribution of the projection from the hippocampal formation to the nucleus accumbens in the rat: an anterograde- and retrograde-horseradish peroxidase study. Neuroscience 7 2321 2335.
24. Kenny P.J. File S.E. Rattray M. 2000 Acute nicotine decreases, and chronic nicotine increases the expression of brain-derived neurotrophic factor mRNA in rat hippocampus. Mol. Brain Res. 85 234 238.
25. Kim M.J. Dunah A.W. Wang Y.T. Sheng M. 2005 Differential roles of NR2A- and NR2B-containing NMDA receptors in Ras-ERK signaling and AMPA receptor trafficking. Neuron 46 745 760.
26. Kim J.J. Fanselow M.S. 1992 Modality-specific retrograde amnesia of fear. Science 256 675 677.
27. Le Foll B. Goldberg S.R. 2005 Nicotine induces conditioned place preferences over a large range of doses in rats. Psychopharmacology 178 481 492.
28. Legault M. Rompre P.P. Wise R.A. 2000 Chemical stimulation of the ventral hippocampus elevates nucleus accumbens dopamine by activating dopaminergic neurons of the ventral tegmental area. J. Neurosci. 20 1635 1642.
29. Levin E.D. Christopher N.C. Briggs S.J. Rose J.E. 1993 Chronic nicotine reverses working memory deficits caused by lesions of the fimbria or medial basalocortical projection. Cognit. Brain Res. 1 137 143.
30. Levin E.D. Simon B.B. 1998 Nicotinic acetylcholine involvement in cognitive function in animals. Psychopharmacology 138 217 230.
31. Levine E.S. Kolb J.E. 2000 Brain-derived neurotrophic factor increases activity of NR2B-containing N-methyl-D-aspartate receptors in excised patches from hippocampal neurons. J. Neurosci. Res. 62 357 362.
32. Lin S.Y. Wu K. Levine E.S. Mount H.T. Suen P.C. Black I.B. 1998 BDNF acutely increases tyrosine phosphorylation of the NMDA receptor subunit 2B in cortical and hippocampal postsynaptic densities. Mol. Brain Res. 55 20 27.
33. Liu L. Wong T.P. Pozza M.F. Lingenhoehl K. Wang Y. Sheng M. Auberson Y.P. Wang Y.T. 2004 Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304 1021 1024.
34. Lu Y.M. Roder J.C. Davidow J. Salter M.W. 1998 Src activation in the induction of long-term potentiation in CA1 hippocampal neurons. Science 279 1363 1367.
35. McQuiston A.R. Madison D.V. 1999 Nicotinic receptor activation excites distinct subtypes of interneurons in the rat hippocampus. J. Neurosci. 19 2887 2896.
36. Monyer H. Burnashev N. Laurie D.J. Sakmann B. Seeburg P.H. 1994 Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12 529 540.
37. Nestler E.J. 2002 Common molecular and cellular substrates of addiction and memory. Neurobiol. Learn. Mem. 78 637 647.
38. Newhouse P.A. Potter A. Lenox R.H. 1993 The effects of nicotinic agents on human cognition: possible therapeutic applications in Alzheimer's and Parkinson's diseases. Med. Chem. Res. 2 628 642.
39. Phillips R.G. LeDoux J.E. 1992 Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 106 274 285.
40. Robbins T.W. Everitt B.J. 2002 Limbic-striatal memory systems and drug addiction. Neurobiol. Learn. Mem. 78 625 636.
41. Role L.W. Berg D.K. 1996 Nicotinic receptors in the development and modulation of CNS synapses. Neuron 16 1077 1085.
42. Saal D. Dong Y. Bonci A. Malenka R.C. 2003 Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron 37 577 582.
43. Salter M.W. Kalia L.V. 2004 Src kinases: a hub for NMDA receptor regulation. Nat. Rev. Neurosci. 5 317 328.
44. Selden N.R. Everitt B.J. Jarrard L.E. Robbins T.W. 1991 Complementary roles for the amygdala and hippocampus in aversive conditioning to explicit and contextual cues. Neuroscience 42 335 350.
45. Sesack S.R. Pickel V.M. 1990 In the rat medial nucleus accumbens, hippocampal and catecholaminergic terminals converge on spiny neurons and are in apposition to each other. Brain Res. 527 266 279.
46. Shalev U. Highfield D. Yap J. Shaham Y. 2000 Stress and relapse to drug seeking in rats: studies on the generality of the effect. Psychopharmacology 150 337 346.
47. Sheng M. Pak D.T. 2000 Ligand-gated ion channel interactions with cytoskeletal and signaling proteins. Annu. Rev. Physiol. 62 755 778.
48. Shoop R.D. Chang K.T. Ellisman M.H. Berg D.K. 2001 Synaptically driven calcium transients via nicotinic receptors on somatic spines. J. Neurosci. 21 771 781.
49. Sudweeks S.N. Yakel J.L. 2000 Functional and molecular characterization of neuronal nicotinic ACh receptors in rat CA1 hippocampal neurons. J. Physiol., (Lond.) 527 515 528.
50. Sun W. Rebec G.V. 2003 Lidocaine inactivation of ventral subiculum attenuates cocaine-seeking behavior in rats. J. Neurosci. 23 10258 10264.
51. Tang Y.P. Shimizu E. Dube G.R. Rampon C. Kerchner G.A. Zhou M. Liu G. Tsien J.Z. 1999 Genetic enhancement of learning and memory in mice. Nature 401 63 69.
52. Thomas M.J. Beurrier C. Bonci A. Malenka R.C. 2001 Long-term depression in the nucleus accumbens: a neural correlate of behavioral sensitization to cocaine. Nat. Neurosci. 4 1217 1223.
53. Thompson A.M. Gosnell B.A. Wagner J.J. 2002 Enhancement of long-term potentiation in the rat hippocampus following cocaine exposure. Neuropharmacology 42 1039 1042.
54. Thompson A.M. Swant J. Gosnell B.A. Wagner J.J. 2004 Modulation of long-term potentiation in the rat hippocampus following cocaine self-administration. Neuroscience 127 177 185.
55. Tovar K.R. Westbrook G.L. 2002 Mobile NMDA receptors at hippocampal synapses. Neuron 34 255 264.
56. Ungless M.A. Whistler J.L. Malenka R.C. Bonci A. 2001 Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 411 583 587.
57. Vorel S.R. Liu X. Hayes R.J. Spector J.A. Gardner E.L. 2001 Relapse to cocaine-seeking after hippocampal theta burst stimulation. Science 292 1175 1178.
58. Wonnacott S. 1997 Presynaptic nicotinic ACh receptors. Trends Neurosci. 20 92 98.
59. Yamazaki Y. Jia Y. Hamaue N. Sumikawa K. 2005 Nicotine-induced switch in the nicotinic cholinergic mechanisms of facilitation of long-term potentiation. Eur. J. Neurosci. 22 845 860.