Nicotine induces glutamate release from thalamocortical terminals in prefrontal cortex

Neuropsychopharmacology

Volumn 28, Issue 2, 2003, Pages 216-225

  Lambe, Evelyn K ^a   Picciotto, Marina R ^a   Aghajanian, George K ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Ectopic action potentials; High affinity nicotinic acetylcholine receptors; Knockout mouse; Lesion; Rat; Spontaneous EPSCs

Indexed keywords

BETA 2 ADRENERGIC RECEPTOR; GLUTAMINE; NICOTINE;

ANIMAL; ARTICLE; DRUG EFFECT; EXCITATORY POSTSYNAPTIC POTENTIAL; IN VITRO STUDY; MALE; METABOLISM; MOUSE; MOUSE MUTANT; PHYSIOLOGY; PREFRONTAL CORTEX; RAT; SECRETION; SPRAGUE DAWLEY RAT; SYNAPTOSOME; THALAMUS;

ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMINE; MALE; MICE; MICE, KNOCKOUT; NICOTINE; PREFRONTAL CORTEX; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, BETA-2; THALAMUS;

EID: 0037310070     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/sj.npp.1300032     Document Type: Article

References (62)

1. Aghajanian GK, Marek GJ (1997). Serotonin induces excitatory postsynaptic potentials in apical dendrites of neocortical pyramidal cells. Neuropharmacology 36: 589-599.
2. Aghajanian GK, Wang RY (1977). Habenular and other midbrain raphe afferents demonstrated by a modified retrograde tracing technique. Brain Res 122: 229-242.
3. Alkondon M, Pereira EFR, Cortes WS, Maelicke A, Albuquerque EX (1997). Choline is a selective agonist of α7 nicotinic acetylcholine receptors in rat brain neurons. Eur J Neurosci 9: 2734-2742.
4. Alkondon M, Pereira EFR, 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.
5. Alkondon M, Rocha ES, Maelicke A, Albuquerque EX (1996). Diversity of nicotinic acetylcholine receptors in rat brain. V. α-bungarotoxin-sensitive nicotinic receptors in olfactory bulb neurons and presynaptic modulation of glutamate release. J Pharmacol Exp Ther 278: 1460-1471.
6. Armitage AK, Dollery CT, George CF, Houseman TH, Lewis PJ, Turner DM (1975). Absorption and metabolism of nicotine from cigarettes. BMJ 4: 313-316.
7. Arnsten AFT, Goldman-Rakic PS (1984). Selective prefrontal cortical projections to the region of the locus coeruleus and raphe in the rhesus monkey. Brain Res 306: 9-18.
8. Berretta N, Jones RS (1996). A comparison of spontaneous EPSCs in layer II and layer IV-V neurons of the rat entorhinal cortex in vitro. J Neurophysiol 76: 1089-1100.
9. Breese CR, Lee MJ, Adams CE, Sullivan B, Logel J, Gillen KM (2000). Abnormal regulation of high affinity nicotinic receptors in subjects with schizophrenia. Neuropsychopharmacology 23: 351-364.
10. Cedarbaum JM, Aghajanian GK (1978). Afferent projections to the rat locus coeruleus as determined by a retrograde tracing technique. J Comp Neurol 178: 1-16.
11. Dalsass M, Kiser S, Mendershausen M, German DC (1981). Medial prefrontal cortical projections to the region of the dorsal periventricular catecholamine system. Neuroscience 6: 657-665.
12. Dani JA (2001). Overview of nicotinic receptors and their roles in the central nervous system. Biol Psychiatry 49: 166-174.
13. Gil Z, Connors BW, Amitai Y (1997). Differential regulation of neocortical synapses by neuromodulators and activity. Neuron 19: 679-686.
14. Gioanni C, Rougeot C, Clarke PBS, Lepouse C, Thierry AM, Vidal C (1999). Nicotinic receptors in the rat prefrontal cortex: increase in glutamate release and facilitation of mediodorsal thalamocortical transmission. Eur J Neurosci 11: 18-30.
15. Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA (1996). Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383: 713-716.
16. Greenland S, Satterfield MH, Lanes SF (1998). A meta-analysis to assess the incidence of adverse effects associated with the transdermal nicotine patch. Drug Saf 18: 297-308.
17. Groenwegen HJ, Berendse HW (1994). The specificity of the ‘nonspecific’ midline and intralaminar thalamic nuclei. Trends Neurosci 17: 52-57.
18. Guo J-Z, Tredway TL, Chiappinelli VA (1998). Glutamate and GABA release are enhanced by different subtypes of presynaptic nicotinic receptors in the lateral geniculate nucleus. J Neurosci 18: 1963-1969.
19. Gutnick MJ, Prince DA (1972). Thalamocortical relay neurons: antidromic invasion of spikes from a cortical epileptogenic focus. Science 176: 424-426.
20. Hajos M, Richards CD, Székely AD, Sharp T (1998). An electrophysiological and neuroanatomical study of the medial prefrontal cortical projection to the midbrain raphe nuclei in the rat. Neuroscience 87: 95-108.
21. Han Z-Y, LeNovere N, Zoli M, Hill JA, Champtiaux N, Changeux JP (2000). Localization of nAChR subunit mRNAs in the brain of Macaca mulatta. Eur J Neurosci 12: 3664-3674.
22. Henningfield JE, Miyasato K, Jasinski DR (1983). Cigarette smokers self-administer intravenous nicotine. Pharmcol Bio-chem Behav 19: 887-890.
23. Himmelheber AM, Sarter M, Bruno JP (2000). Increases in cortical acetylcholine release during sustained attention performance in rats. Cog Brain Res 9: 313-325.
24. Lambe EK, Aghajanian GK (2001). The role of Kv.12-containing potassium channels in serotonin-induced glutamate release from thalamocortical terminals in rat frontal cortex. J Neurosci 21: 9955-9963.
25. Lavine N, Reuben M, Clarke PBS (1997). A population of nicotinic receptors is associated with thalamocortical afferents in the adult rat: laminal and areal analysis. J Comp Neurol 380: 175-190.
26. Léna C, Changeux J-P (1997). Role of Ca2+ ions in nicotinic facilitation of GABA release in mouse thalamus. J Neurosci 17: 576-585.
27. Léna C, Changeux J-P, Mulle C (1993). Evidence for ‘pretermi-nal’nicotinic receptors on GABAergic axons in the rat interpeduncular nucleus. J Neurosci 13: 2680-2688.
28. Levin ED, Simon BB (1998). Nicotinic acetylcholine involvement in cognitive function in animals. Psychopharmacology 138: 217-230.
29. Li X, Rainnie DG, McCarley RW, Greene RW (1998). Presynaptic nicotinic receptors facilitate monoaminergic transmission. J Neurosci 18: 1904-1912.
30. Luppi P-H, Aston-Jones G, Akaoka H, Chouvet G, Jouvet M (1995). Afferent projections to the rat locus coeruleus demonstrated by retrograde and anterograde tracing with cholera-toxin B subunit and phaseolus vulgaris leucoagglutinin. Neuroscience 65: 119-160.
31. MacDermott AB, Role LW, Siegelbaum SA (1999). Presynaptic ionotropic receptors and the control of transmitter release. Annu Rev Neuroscience 22: 443-485.
32. Marek GJ, Aghajanian GK (1998). 5-Hydroxytryptamine-induced excitatory postsynaptic currents in neocortical layer V pyramidal cells: suppression by m-opiate receptor activation. Neuroscience 86: 485-497.
33. Marek GJ, Wright RA, Gewirtz JC, Schoepp DD (2001). A major role for thalamocortical afferents in serotonergic hallucinogen receptor function in the rat neocortex. Neuroscience 105: 379-392.
34. Marubio LM, del Mar Arroyo-Jimenez M, Cordero-Erausquin M, Lé na C, Le Novere N, de Kerchove d’Exaerde A (1999). Reduced antinociception in mice lacking neuronal nicotinic receptor subunits. Nature 398: 805-810.
35. McCormick DA, Contreras D (2001). On the cellular and network bases of epileptic seizures. Annu Rev Physiol 63: 815-846.
36. McGehee D, Heath M, Gelber S, Devay P, Role LW (1995). Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 269: 1692-1697.
37. Neafsey EJ, Hurley-Guis KM, Arvantis D (1986). The topographical organization of neurons in the rat medial frontal, insular and olfactory cortex projecting to the solitary nucleus, olfactory bulb, periaqueductal gray and superior colliculus. Brain Res 377: 261-270.
38. Noebels JL, Prince DA (1978). Development of focal seizures in cerebral cortex: role of axon terminal bursting. J Neurophysiol 41: 1267-1281.
39. Passetti F, Dalley JW, O’Connell MT, Everitt BJ, Robbins TW (2000). Increased acetylcholine release in the rat medial prefrontal cortex during performance of a visual attentional task. Eur J Neurosci 12: 3051-3058.
40. Paxinos G, Watson C (1986). The Rat Brain in Stereotaxic Coordinates. Academic Press: New York.
41. Peoples LL (2002). Will, anterior cingulate cortex, and addiction. Science 296: 1623-1624.
42. Perry EK, Lee MLW, Martin-Ruiz CM, Court JA, Volsen SG, Merrit J (2001). Cholinergic activity in autism: abnormalities in the cerebral cortex and basal forebrain. Am J Psychiatry 158: 1058-1066.
43. Peyron C, Petit J-M, Rampon C, Jouvet M, Luppi P-H (1998). Forebrain afferents to the rat dorsal raphe nucleus demonstrated by retrograde and anterograde tracing methods. Neuroscience 82: 443-468.
44. Picciotto MR, Zoli M, Leéna C, Bessis A, Lallemand Y, LeNovere N (1995). Abnormal avoidance learning in mice lacking functional high-affinity nicotine receptor in the brain. Nature 374: 65-67.
45. Pinault D (1990). Antidromic firing occurs spontaneously on thalamic relay neurons: triggering of ectopic action potentials by somatic intrinsic burst discharges. Neuroscience 34: 281-292.
46. Pinault D (1995). Backpropagation of action potentials generated at ectopic axonal loci: hypothesis that axon terminals integrate local environmental signals. Brain Res Rev 21: 42-92.
47. Pinault D, Pumain R (1989). Antidromic firing occurs spontaneously on thalamic relay neurons: triggering of somatic intrinsic burst discharges by ectopic action potentials. Neuroscience 31: 625-637.
48. Prusky GT, Shaw C, Cynader MS (1987). Nicotine receptors are located on lateral geniculate nucleus terminals in cat visual cortex. Brain Res 412: 131-138.
49. Rosen AD, Vastola EF (1977). Antidromic activity in visual radiation during evoked cortical responses. J Neurophysiol 40: 9-14.
50. Rumsey JM, Ernst M (2000). Functional neuroimaging of autistic disorders. Ment Retard Dev Disabil Res Rev 6: 171-179.
51. Sahin M, Bowen WD, Donoghue JP (1992). Location of nicotinic and muscarinic cholinergic and m-opiate receptors in rat cerebral neocortex: evidence from thalamic and cortical lesions. Brain Res 579: 135-147.
52. Schwarztkroin PA, Mutani R, Prince DA (1975). Orthodromic and antidromic effects of a cortical epileptiform focus on ventrolateral nucleus of the cat. J Neurophysiol 38: 795-811.
53. Shidara M, Richmond BJ (2002). Anterior cingulate: single neuronal signals related to degree of reward expectancy. Science 296: 1709-1711.
54. Sidach SS, Mintz IM (2000). Low-affinity blockade of neuronal N-type Ca2+ channels by the spider toxin o-agatoxin-IVA. J Neurosci 20: 7174-7182.
55. Stasheff SF, Hines M, Wilson MA (1993). Axon terminal hyperexcitability associated with epileptogenesis in vitro. I. Origin of ectopic spikes. J Neurophysiol 70: 961-975.
56. Stein EA, Pankiewicz J, Harsch HH, Cho J-K, Fuller SC, Hoffmann RG (1998). Nicotine-induced limbic cortical activation in the human brain: a functional MRI study. Am J Psychiat 155: 1009-1015.
57. Vidal C, Changeux J-P (1993). Nicotinic and muscarinic modulations of excitatory synaptic transmission in the rat prefrontal cortex in vitro. Neuroscience 56: 23-32.
58. Wada E, Wada K, Boulter J, Deneris E, Heinemann S, Patrick J (1989). Distribution of a2, a3, a4, and ß2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: a hybridization histochemical study in the rat. J Comp Neurol 184: 314-335.
59. Weinberger DR, Berman KF (1996). Prefrontal function in schizophrenia: confounds and controversies. Philos Trans R Soc London 351: 1495-1503.
60. Wong TP, Marchese G, Casu MA, Ribeiro-da-Silva A, Cuello AC, De Koninck Y (2000). Loss of presynaptic and postsynaptic structures is accompanied by compensatory increase in action potential-dependent synaptic input to layer V neocortical pyramidal neurons in aged rats. J Neurosci 20: 8596-8606.
61. Zoli M, Jansson A, Sykova E, Agnati LF, Fuxe K (1999). Volume transmission in the CNS and its relevance for neuropsychopharmacology. Trends Pharmacol Sci 20: 142-150.
62. Zoli M, Lé na C, Picciotto MR, Changeux JP (1998). Identification of four classes of brain nicotinic receptors using ß2 mutant mice. J Neurosci 18: 4461-4472.