Activation of presynaptic α7 nicotinic receptors evokes an excitatory response in hippocampal CA3 neurones in anaesthetized rats: An in vivo iontophoretic study

British Journal of Pharmacology

Volumn 159, Issue 3, 2010, Pages 554-565

  Huang, Lan Ting ^a   Sherwood, John L ^b,c   Sun, Ya Jie ^a   Lodge, David ^b,c   Wang, Yun ^a,c  

^a FUDAN UNIVERSITY   (China)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c ELI LILLY AND COMPANY   (United States)

Author keywords

AR R17779; CA3; Hippocampus; Iontophoresis; Nicotine; Presynaptic 7 nAChR; PSAB OFP; Rat

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 5' PHENYLSPIRO[1 AZABICYCLO[2.2.2]OCTANE 3,2' (3'H)FURO[2,3 B]PYRIDINE; 6,7 DINITRO 2,3 QUINOXALINEDIONE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AR R17779; BUNGAROTOXIN RECEPTOR; GLUTAMIC ACID; METHYLLYCACONITINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NICOTINE; NICOTINIC AGENT; UNCLASSIFIED DRUG; 5' PHENYLSPIRO(1 AZABICYCLO(2.2.2.))OCTANE 3,2' (3'H)FURO(2,3 B)PYRIDINE; 5'-PHENYLSPIRO(1-AZABICYCLO(2.2.2.))OCTANE-3,2'-(3'H)FURO(2,3-B)PYRIDINE; ACONITINE; AR-R 17779; BRIDGED COMPOUND; DEXTRO ASPARTIC ACID; DRUG DERIVATIVE; FUSED HETEROCYCLIC RINGS; N METHYLASPARTIC ACID; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR BLOCKING AGENT; PRESYNAPTIC RECEPTOR; PYRIDINE; PYRIDINE DERIVATIVE; QUINOXALINE DERIVATIVE; SPIRO COMPOUND; SPIRO[1 AZABICYCLO[2.2.2]OCTANE 3,2' THIAZOLIDINE] 2' ONE;

ANESTHESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; ELECTRIC CURRENT; EXTRACELLULAR SPACE; HIPPOCAMPUS; IN VIVO STUDY; IONTOPHORESIS; LEARNING; MALE; MEMORY; NERVE EXCITABILITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; ANIMAL; CYTOLOGY; DRUG EFFECT; METABOLISM; NERVE CELL; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

2-AMINO-5-PHOSPHONOVALERATE; ACONITINE; ANIMALS; BICYCLO COMPOUNDS, HETEROCYCLIC; BRIDGED COMPOUNDS; D-ASPARTIC ACID; GLUTAMIC ACID; HIPPOCAMPUS; MALE; N-METHYLASPARTATE; NEURONS; NICOTINE; NICOTINIC ANTAGONISTS; PYRIDINES; QUINOXALINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NICOTINIC; RECEPTORS, PRESYNAPTIC; SPIRO COMPOUNDS;

EID: 76449104246     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2009.00529.x     Document Type: Article

References (52)

1. Alexander SPH, Mathie A, Peters JA (2008). Guide to Receptors and Channels (GRAC). Br J Pharmacol 153 (Suppl. 2 S1 S209.
2. Alkondon M, Albuquerque EX (2001). Nicotinic acetylcholine receptor alpha 7 and alpha4beta2 subtypes differentially control GABAergic input to CA1 neurons in rat hippocampus. J Neurophysiol 86 : 3043 3055.
3. Alkondon M, Albuquerque EX (2004). The nicotinic acetylcholine receptor subtypes and their function in the hippocampus and cerebral cortex. Prog Brain Res 145 : 109 120.
4. Alkondon M, Pereira EF, Albuquerque EX (1996). Mapping the location of functional nicotinic and gamma-aminobutyric acidA receptors on hippocampal neurones. JPET 279 : 1491 1506.
5. Alkondon M, Pereira EF, Barbosa CT, Albuquerque EX (1997). Neuronal nicotinic acetylcholine receptor activation modulates gammaaminobutyric acid release from CA1 neurons of rat hippocampal slices. JPET 283 : 1396 1411.
6. Alkondon M, Pereira EF, Eisenberg HM, Albuquerque EX (1999). Choline and selective antagonists identify two subtypes of nicotinic acetylcholine receptors that modulate GABA release from CA1 interneurons in rat hippocampal slices. J Neurosci 19 : 2693 2705.
7. Alkondon M, Pereira EFR, Almedia LEF, Randall WRR, Albuquerque EX (2000). Nicotine at concentrations found in cigarette smokers activates and desensitizes nicotinic acetylcholine receptors in CA1 interneurons of rat hippocampus. Neuropharmacology 39 : 2726 2739.
8. Astles PC, Baker SR, Boot JR, Broad LM, Dell CP, Keenan M (2002). Recent progress in the development of subtype selective nicotinic acetylcholine receptor ligands. Curr Drug Targets CNS Neurol Disord 1 : 337 348.
9. Buccafusco JJ, Letchworth SR, Bencherif M, Lippiello PM (2005). Long-lasting cognitive improvement with nicotinic receptor agonists: mechanisms of pharmacokinetic-pharmacodynamic discordance. TIPS 26 : 352 360.
10. Broad LM, Felthouse C, Zwart R, Mcphie GI, Pearson KH, Craig PJ et al. (2002). PSAB-OFP, a selective α7 nicotinic receptor agonist, is also a potent agonist of the 5-HT3 receptor. Eur J Pharmacol 452 : 137 144.
11. Couturier S, Bertrand D, Matter JM, Hernandez MC, Bertrand S, Millar N et al. (1990). A neuronal nicotinic acetylcholine receptor subunit (alpha 7) is developmentally regulated and forms a homo-oligomeric channel blocked by alpha-BTX. Neuron 5 : 847 856.
12. Durany N, Zochling R, Boissl KW, Paulus W, Ransmayr G, Tatschner T et al. (2000). Human post-mortem striatal alpha4beta2 nicotinic acetylcholine receptor density in schizophrenia and Parkinson's syndrome. Neurosci Lett 287 : 109 112.
13. Fabian-Fine R, Skehel P, Errington ML, Davies HA, Sher E, Stewart MG et al. (2001). Ultrastructural distribution of the alpha7 nicotinic acetylcholine receptor subunit in rat hippocampus. J Neurosci 21 : 7993 8003.
14. Frazier CJ, Rollins YD, Hall ME, Young DA, Rose GM (1996). Cholinergic deafferentation enhances rat hippocampal pyramidal neuron responsiveness to locally applied nicotine. Brain Res 727 : 217 220.
15. Frazier CJ, Rollins YD, Breese CR, Leonard S, Freedman R, Dunwiddie TV (1998). Acetylcholine activates an alpha-bungarotoxin-sensitive nicotinic current in rat hippocampal interneurons, but not pyramidal cells. J Neurosci 18 : 1187 1195.
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. Fujii S, Jia YS, Yan AZ, Sumikawa K (2000). Nicotine reverses GABAergic inhibition of long-term potentiation induction in the hippocampal CA1 region. Brain Res 863 : 259 265.
18. Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA (1996). Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383 : 713 716.
19. Hunter BE, de Fiebre CM, Papke R, Kem WR, Meyer EM (1994). A novel nicotinic agonist facilitates induction of long-term potentiation in the rat hippocampus. Neurosci Lett 168 : 130 134.
20. 1D receptors in the rat nucleus tractus solitarius: opposing action on neurons that receive an excitatory vagal C-fibre afferent input. Br J Pharmacol 150 : 987 995.
21. Ji K, Dani JA (2000). Inhibition and disinhibition of pyramidal neurons by activation of nicotinic receptors on hippocampal interneurons. J Neurophysiol 83 : 2682 2690.
22. Ji D, Lape R, Dani JA (2001). Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity. Neuron 31 : 131 141.
23. Jones S, Yakel JL (1997). Functional nicotinic Ach receptors on interneurones in the rat hippocampus. J Physiol 504 : 603 610.
24. Kasa P (1986). The cholinergic systems in brain and spinal cord. Prog Neurobiol 26 : 211 272.
25. Leonard S, Breese C, Adams C, Benhammou K, Gault J, Stevens K et al. (2000). Smoking and schizophrenia: abnormal nicotinic receptor expression. Eur J Pharmacol 393 : 237 242.
26. Levin ED (1992). Nicotinic systems and cognitive function. Psychopharmacology 108 : 417 431.
27. Levin ED, Bettegowda C, Blosser J, Gordon J (1999). AR-R17779, an α7 nicotinic agonist, improves learning and memory in rats. Behav Pharmacol 10 : 675 680.
28. Li X, Rainnie DG, McCarley RW, Greene RW (1998). Presynaptic nicotinic receptors facilitate monoaminergic transmission. J Neurosci 18 : 1904 1912.
29. Maggi L, Sher E, Cherubini E (2001). Regulation of GABA release by nicotinic acetylcholine receptors in the neonatal rat hippocampus. J Physiol 536 : 89 100.
30. Maggi L, Le Magueresse C, Changeux JP, Cherubini E (2003). Nicotine activates immature 'silent' connections in the developing hippocampus. Proc Natl Acad Sci U S A 100 : 2059 2064.
31. Matsuyama S, Matsumoto A, Enomoto T, Nishizaki T (2000). Activation of nicotinic acetylcholine receptors induces long-term potentiation in vivo in the intact mouse dentate gyrus. Eur J Neurosci 12 : 3741 3747.
32. Moore C, Wang Y, Ramage AG (2008). Cardiovascular effects of activation of central α7 and α4β2 nAChRs: A role for vasopressin in anaesthetized rats. Br J Pharmacol 153 : 1728 1738.
33. Mullen G, Napier J, Balestra M, DeCory T, Hale G, Macor J et al. (2000). Spiro[1-azabicyclo[2.2.2]octane-3,5′-oxazolidin-2′-one], a conformationally restricted analogue of acetylcholine, is a highly selective full agonist at the alpha 7 nicotinic acetylcholine receptor. J Med Chem 43 : 4045 4050.
34. Nakauchi S, Brennan RJ, Boulter J, Sumikawa K (2007). Nicotine gates long-term potentiation in the hippocampal CA1 region via the activation of α2* nicotinic ACh receptors. Eur J Neurosci 25 : 2666 2681.
35. Paterson D, Nordberg A (2000). Neuronal nicotinic receptors in the human brain. Prog Neurobiol 61 : 75 111.
36. Paxinos G, Watson C (1986). The Rat Brain in Stereotaxic Coordinates, 2nd edn. Academic Press Inc : San Diego, CA.
37. Prendergast MA, Terry AV Jr., Jackson WJ, Marsh KC, Decker MW, Arneric SP et al. (1997). Improvement in accuracy of delayed recall in aged and non-aged mature monkeys after intramuscular or transdermal administration of the CNS nicotinic receptor agonist abt-418. Psychopharmacology 130 : 276 284.
38. Radcliffe KA, Dani JA (1998). Nicotinic stimulation produces multiple forms of increased glutamatergic synaptic transmission. J Neurosci 18 : 7075 7083.
39. Rezvani AH, Levin ED (2001). Cognitive effects of nicotine. Biol Psychiatry 49 : 258 267.
40. Schilstrom B, Svensson HM, Svensson TH, Nomikos GG (1998). Nicotine and food induced dopamine release in the nucleus accumbens of the rat: putative role of alpha7 nicotinic receptors in the ventral tegmental area. Neuroscience 85 : 1005 1009. (Pubitemid 28293408)
41. Seguela 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.
42. Sharma G, Vijayaraghavan S (2003). Modulation of presynaptic store calcium induces release of glutamate and postsynaptic firing. Neuron 38 : 929 939.
43. Sharma G, Grybko M, Vijayaraghavan S (2008). Action potential-independent and nicotinic receptor-mediated concerted release of multiple quanta at hippocampal CA3-mossy fiber synapses. J Neurosci 28 : 2563 2575.
44. Sudweeks SN, Yakel JL (2000). Functional and molecular characterization of neuronal nicotinic ACh receptors in rat CA1 hippocampal neurons. J Physiol 527 : 515 528.
45. Summers KL, Kem WR, Giacobini E (1997). Nicotinic agonist modulation of neurotransmitter levels in the rat frontoparietal cortex. Jpn J Pharmacol 74 : 139 146.
46. Wanaverbecq N, Semyanov A, Pavlov I, Walker MC, Kullmann DM (2007). Cholinergic axons modulate GABAergic signaling among hippocampal interneurons via postsynaptic α7 nicotinic receptors. J Neurosci 27 : 5683 5693.
47. Wang Y, Sherwood JL, Mile CP, Whiffin G, Lodge D (2006a). TC-2559 excites dopaminergic neurones in the ventral tegmental area by stimulating alpha4beta2-like nicotinic acetylcholine receptors in anaesthetised rats. Br J Pharmacol 147 : 379 390.
48. Wang Y, Sherwood JL, Lodge D (2006b). The α4β2 nicotinic acetylcholine receptor agonist TC-2559 impairs long-term potentiation in the dentate gyrus in vivo. Neurosci Lett 406 : 183 188.
49. White HK, Levin ED (2004). Chronic transdermal nicotine patch treatment effects on cognitive performance in age-associated memory impairment. Psychopharmacology 171 : 465 471.
50. Wittner L, Henze DA, Záborszky L, Buzsáki G (2007). Three-dimensional reconstruction of the axon arbor of a CA3 pyramidal cell recorded and filled in vivo. Brain Struct Funct 21 : 75 83.
51. Yamazaki Y, Jia Y, Hamaue N, Sumikawa K (2005). Nicotine-induced switch in the nicotinic cholinergic mechanisms of facilitation of long-term potentiation induction. Eur J Neurosci 22 : 845 860.
52. Yoshida K, Oka H (1995). Topographical projections from the medial septum-diagonal band complex to the hippocampus: a retrograde tracing study with multiple fluorescent dyes in rats. Neurosci Res 21 : 199 209.