Selective excitation of subtypes of neocortical interneurons by nicotinic receptors

Journal of Neuroscience

Volumn 19, Issue 13, 1999, Pages 5228-5235

  Porter, James T ^a,b   Cauli, Bruno ^a   Tsuzuki, Keisuke ^a   Lambolez, Bertrand ^a   Rossier, Jean ^a   Audinat, Etienne ^a  

^a Brain Plasticity Unit   (France)

^b WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

Acetylcholine; Calcium binding proteins; Dihydro erythroidine; Mecamylamine; Methyllycaconitine; Neuropeptides; Single cell PCR

Indexed keywords

4 AMINOBUTYRIC ACID; ACETYLCHOLINE; CALCIUM ION; CHOLECYSTOKININ; DIHYDRO BETA ERYTHROIDINE; GLUTAMIC ACID; MECAMYLAMINE; METHYLLYCACONITINE; MUSCARINIC RECEPTOR BLOCKING AGENT; NICOTINIC AGENT; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR BLOCKING AGENT; SOMATOSTATIN; TETRODOTOXIN; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL TISSUE; ARTICLE; BRAIN BLOOD FLOW; BRAIN METABOLISM; BRAIN SLICE; CONTROLLED STUDY; EXTRACELLULAR CALCIUM; INTERNEURON; NEOCORTEX; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EID: 0033168758     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-13-05228.1999     Document Type: Article

References (63)

1. 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.
2. Angulo MC, Lambolez B, Audinat E, Hestrin S, Rossier J (1997) Subunit composition, kinetic, and permeation properties of AMPA receptors in single neocortical nonpyramidal cells. J Neurosci 17:6685-6696.
3. Boulter J, O'Shea-Greenfield A, Duvoisin RM, Connolly JG, Wada E, Jensen A, Gardner PD, Ballivet M, Deneris ES, McKinnon D (1990) α3, α5, and β4: three members of the rat neuronal nicotinic acetylcholine receptor-related gene family form a gene cluster. J Biol Chem 265:4472-4482.
4. Cauli B, Audinat E, Lambolez B, Angulo M-C, Ropert N, Tsuzuki K, Hestrin S, Rossier J (1997) Molecular and physiological diversity of cortical nonpyramidal cells. J Neurosci 17:3894-3906.
5. Changeux JP, Bertrand D, Corringer PJ, Dehaene S, Edelstein S, Lena C, Le Novere N, Marubio L, Picciotto M, Zoli M (1998) Brain nicotinic receptors: structure and regulation, role in learning and reinforcement. Brain Res Brain Res Rev 26:198-216.
6. Chédotal A, Cozzari C, Faure MP, Hartman BK, Hamel E (1994a) Distinct choline acetyltransferase (ChAT) and vasoactive intestinal polypeptide (VIP) bipolar neurons project to local blood vessels in the rat cerebral cortex. Brain Res 646:181-193.
7. Chédotal A, Umbriaco D, Descarries L, Hartman BK, Hamel E (1994b) Light and electron microscopic immunocytochemical analysis of the neurovascular relationships of choline acetyltransferase and vasoactive intestinal polypeptide nerve terminals in the rat cerebral cortex. J Comp Neurol 343:57-71.
8. Connor JR, Peters A (1984) Vasoactive intestinal polypeptide-immunoreactive neurons in rat visual cortex. Neuroscience 12:1027-1044.
9. Cooper E, Couturier S, Ballivet M (1991) Pentameric structure and subunit stoichiometry of a neuronal nicotinic acetylcholine receptor. Nature 350:235-238.
10. Couturier S, Bertrand D, Matter JM, Hernandez MC, Bertrand S, Millar N, Valera S, Barkas T, Ballivet M (1990) A neuronal nicotinic acetylcholine receptor subunit (α7) is developmentally regulated and forms a homo-oligomeric channel blocked by α-BTX. Neuron 5:847-856.
11. Eberling JL, Jagust WJ, Reed BR, Baker MG (1992) Reduced temporal lobe blood flow in Alzheimer's disease. Neurobiol Aging 13:483-491.
12. Eckenstein F, Baughman RW (1984) Two types of cholinergic innervation in cortex, one co-localized with vasoactive intestinal polypeptide. Nature 309:153-155.
13. Elgoyhen AB, Johnson DS, Boulter J, Vetter DE, Heinemann S (1994) α9: an acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells. Cell 79:705-715.
14. Frazier CJ, Rollins YD, Breese CR, Leonard S, Freedman R, Dunwiddie TV (1998) Acetylcholine activates an α-bungarotoxin-sensitive nicotinic current in rat hippocampal interneurons, but not pyramidal cells. J Neurosci 18:1187-1195.
15. Gil Z, Connors BW, Amitai Y (1997) Differential regulation of neocortical synapses by neuromodulators and activity. Neuron 19:679-686.
16. Gitelman DR, Prohovnik I (1992) Muscarinic and nicotinic contributions to cognitive function and cortical blood flow. Neurobiol Aging 13:313-318.
17. Granon S, Poucet B, Thinus-Blanc C, Changeux JP, Vidai C (1995) Nicotinic and muscarinic receptors in the rat prefrontal cortex: differential roles in working memory, response selection and effortful processing, Psychopharmacology 119:139-144.
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. Hendry SH, Jones EG, Beinfeld MC (1983) Cholecystokinin-immunoreactive neurons in rat and monkey cerebral cortex make symmetric synapses and have intimate associations with blood vessels. Proc Natl Acad Sci USA 80:2400-2404.
20. Itakura T, Yokote H, Okuno T, Naka Y, Nakakita K, Kamei I, Nakai K, Imai H, Komai N (1987) Regulation of rCBF by intracortical vasoactive intestinal polypeptide-containing neurons. Immunohistochemical and hydrogen clearance study in rats. J Neurosurg 67:93-96.
21. Jones S, Yakel JL (1997) Functional nicotinic ACh receptors on interneurones in the rat hippocampus. J Physiol (Lond) 504:603-610.
22. Kawaguchi Y (1995) Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci 15:2638-2655.
23. Kawaguchi Y, Kubota Y (1996) Physiological and morphological identification of somatostatin-or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex. J Neurosci 16:2701-2715.
24. Kubota Y, Kawaguchi Y (1997) Two distinct subgroups of cholecystokinin-immunoreactive cortical interneurons. Brain Res 752:175-183.
25. Kubota Y, Hattori R, Yui Y (1994) Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex. Brain Res 649:159-173.
26. Lambolez B, Audinat E, Bochet P, Crépel F, Rossier J (1992) AMPA receptor subunits expressed by single Purkinje cells. Neuron 9:247-258.
27. Le Novere N, Changeux JP (1995) Molecular evolution of the nicotinic acetylcholine receptor: an example of multigene family in excitable cells. J Mol Evol 40:155-172.
28. Lena C, Changeux JP (1997) Pathological mutations of nicotinic receptors and nicotine-based therapies for brain disorders. Curr Opin Neurobiol 7:674-682.
29. Luetje CW, Patrick J (1991) Both α-and β-subunits contribute to the agonist sensitivity of neuronal nicotinic acetylcholine receptors. J Neurosci 11:837-845.
30. Magistretti PJ (1990) VIP neurons in the cerebral cortex. Trends Pharmacol Sci 11:250-254.
31. Magistretti PJ, Morrison JH, Shoemaker WJ, Sapin V, Bloom FE (1981) Vasoactive intestinal polypeptide induces glycogenolysis in mouse cortical slices: a possible regulatory mechanism for the local control of energy metabolism. Proc Natl Acad Sci USA 78:6535-6539.
32. Magistretti PJ, Morrison JH, Shoemaker WJ, Bloom FE (1984) Morphological and functional correlates of VIP neurons in cerebral cortex. Peptides 5:213-218.
33. McCormick DA, Connors BW, Lighthall JW, Prince DA (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54:782-806.
34. 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.
35. Morrison JH, Magistretti PJ, Benoit R, Bloom FE (1984) The distribution and morphological characteristics of the intracortical VIP-positive cell: an immunohistochemical analysis. Brain Res 292:269-282.
36. 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.
37. Palma E, Bertrand S, Binzoni T, Bertrand D (1996) Neuronal nicotinic α7 receptor expressed in Xenopus oocytes presents five putative binding sites for methyllycaconitine. J Physiol (Lond) 491:151-161.
38. Papadopoulos GC, Parnavelas JG, Cavanagh ME (1987) Extensive coexistence of neuropeptides in the rat visual cortex. Brain Res 420:95-99.
39. Papke RL (1993) The kinetic properties of neuronal nicotinic receptors: genetic basis of functional diversity. Prog Neurobiol 41:509-531.
40. Papke RL, Boulter J, Patrick J, Heinemann S (1989) Single-channel currents of rat neuronal nicotinic acetylcholine receptors expressed in Xenopus oocytes. Neuron 3:589-596.
41. Parks RW, Becker RE, Rippey RF, Gilbert DG, Matthews JR, Kabatay E, Young CS, Vohs C, Danz V, Keim P, Collins GT, Zigler SS, Urycki PG (1996) Increased regional cerebral glucose metabolism and semantic memory performance in Alzheimer's disease: a pilot double blind transdermal nicotine positron emission tomography study. Neuropsychol Rev 6:61-79.
42. Porter JT, Cauli B, Staiger JF, Lambolez B, Rossier J, Audinat E (1998) Properties of bipolar VIPergic interneurons and their excitation by pyramidal neurons in the rat neocortex. Eur J Neurosci 10:3617-3628.
43. Ramirez-Latorre J, Yu CR, Qu X, Perin F, Karlin A, Role L (1996) Functional contributions of α5 subunit to neuronal acetylcholine receptor channels. Nature 380:347-351.
44. Roerig B, Nelson DA, Katz LC (1997) Fast synaptic signaling by nicotinic acetylcholine and serotonin 5-HT3 receptors in developing visual cortex. J Neurosci 17:8353-8362.
45. Role LW, Berg DK (1996) Nicotinic receptors in the development and modulation of CNS synapses. Neuron 16:1077-1085.
46. Ruano D, Lambolez B, Rossier J, Paternain AV, Lerma J (1995) Kainate receptor subunits expressed in single cultured hippocampal neurons: molecular and functional variants by RNA editing. Neuron 14:1009-1017.
47. Sanberg PR, Silver AA, Shytle RD, Philipp MK, Cahill DW, Fogelson HM, McConville BJ (1997) Nicotine for the treatment of Tourette's syndrome. Pharmacol Ther 74:21-25.
48. Sanberg PR, Shytle RD, Silver AA (1998) Treatment of Tourette's syndrome with mecamylamine [letter]. Lancet 352:705-706.
49. Sargent PB (1993) The diversity of neuronal nicotinic acetylcholine receptors. Annu Rev Neurosci 16:403-443.
50. Sivilotti L, Colquhoun D (1995) Acetylcholine receptors: too many channels, too few functions. Science 269:1681-1682.
51. Steinlein OK, Mulley JC, Propping P, Wallace RH, Phillips HA, Sutherland GR, Scheffer IE, Berkovic SF (1995) A missense mutation in the neuronal nicotinic acetylcholine receptor α4 subunit is associated with autosomal dominant nocturnal frontal lobe epilepsy. Nat Genet 11:201-203.
52. Swerdlow R, Marcus DL, Landman J, Kooby D, Frey W, Freedman ML (1994) Brain glucose metabolism in Alzheimer's disease. Am J Med Sci 308:141-144.
53. Thomson AM, Deuchars J (1994) Temporal and spatial properties of local circuits in neocortex. Trends Neurosci 17:119-126.
54. Uchida S, Kagitani F, Nakayama H, Sato A (1997) Effect of stimulation of nicotinic cholinergic receptors on cortical cerebral blood flow and changes in the effect during aging in anesthetized rats. Neurosci Lett 228:203-206.
55. Vidai C, Changeux JP (1993) Nicotinic and muscarinic modulations of excitatory synaptic transmission in the rat prefrontal cortex in vitro. Neuroscience 56:23-32.
56. 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.
57. Wada E, McKinnon D, Heinemann S, Patrick J, Swanson LW (1990) The distribution of mRNA encoded by a new member of the neuronal nicotinic acetylcholine receptor gene family (α5) in the rat central nervous system. Brain Res 526:45-53.
58. 3H]nicotinic acetylcholine binding in Alzheimer's disease and Parkinson's disease: an autoradiographic study. Neurology 38:720-723.
59. Wilson K, Bowen D, Francis P, Tyrrell P (1991) Effect of central cholinergic stimulation on regional cerebral blood flow in Alzheimer's disease. Br J Psychiatry 158:558-562.
60. Xiang Z, Huguenard JR, Prince DA (1998) Cholinergic switching within neocortical inhibitory networks. Science 281:985-988.
61. Yaksh TL, Wang JY, Go VL (1987) Cortical vasodilatation produced by vasoactive intestinal polypeptide (VIP) and by physiological stimuli in the cat. J Cereb Blood Flow Metab 7:315-326.
62. Yu CR, Role LW (1998) Functional contribution of the α5 subunit to neuronal nicotinic channels expressed by chick sympathetic ganglion neurones. J Physiol (Lond) 509:667-681.
63. Zoli M, Lena C, Picciotto MR, Changeux JP (1998) Identification of four classes of brain nicotinic receptors using β2 mutant mice. J Neurosci 18:4461-4472.