Nicotine exposure refines visual map topography through an NMDA receptor-mediated pathway

European Journal of Neuroscience

Volumn 24, Issue 11, 2006, Pages 3026-3042

  Yan, Xiaohua ^a   Zhao, Bing ^a,b   Butt, Christopher M ^a,c   Debski, Elizabeth A ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c WEST VIRGINIA SCHOOL OF OSTEOPATHIC MEDICINE   (United States)

Author keywords

Acetylcholine; Frog; Nicotinic receptor; Optic tectum; Retinal ganglion cell

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; ALPHA BUNGAROTOXIN; ANATOXIN A; DIZOCILPINE; EPIBOXIDINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NICOTINE; NICOTINIC AGENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN MAPPING; CONCENTRATION RESPONSE; CONTROLLED STUDY; FROG; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; NONHUMAN; OPTIC TECTUM; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RETINA GANGLION CELL; RETINOTECTAL PROJECTION; TISSUE DISTRIBUTION; VISUAL SYSTEM;

ACETYLCHOLINE; AGING; ANIMALS; AXONS; BRAIN MAPPING; CELL DIFFERENTIATION; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; IMMUNOHISTOCHEMISTRY; NEURONAL PLASTICITY; NICOTINE; NICOTINIC AGONISTS; RANA PIPIENS; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, NICOTINIC; RETINA; RETINAL GANGLION CELLS; SUPERIOR COLLICULUS; SYNAPTIC TRANSMISSION; VISUAL PATHWAYS;

EID: 33845652292     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2006.05204.x     Document Type: Article

References (93)

1. Aizenman, E., Loring, R.H. & Lipton, S.A. (1990) Blockade of nicotinic responses in rat retinal ganglion cells by neuronal bungarotoxin. Brain Res., 517, 209-214.
2. Amador, M. & Dani, J.A. (1991) MK-801 inhibition of nicotinic acetylcholine receptor channels. Synapse, 7, 207-215.
3. Bednar, J.A., Kelkar, A. & Miikkulainen, R. (2004) Scaling self-organizing maps to model large cortical networks. Neuroinformatics, 2, 275-302.
4. Britto, L.R., Hamassaki-Britto, D.E., Ferro, E.S., Keyser, K.T., Karten, H.J. & Lindstrom, J.M. (1992) Neurons of the chick brain and retina expressing both alpha-bungarotoxin-sensitive and alpha-bungarotoxin-insensitive nicotinic acetylcholine receptors: an immunohistochemical analysis. Brain Res., 590, 193-200.
5. Britto, L.R., Torrao, A.S., Hamassaki-Britto, D.E., Mpodozis, J., Keyser, K.T., Lindstrom, J.M. & Karten, H.J. (1994) Effects of retinal lesions upon the distribution of nicotinic acetylcholine receptor subunits in the chick visual system. J. Comp. Neurol., 350, 473-484.
6. Buisson, B. & Bertrand, D. (2001) Chronic exposure to nicotine upregulates the human (alpha) 4 (beta) 2 nicotinic acetylcholine receptor function. J. Neurosci., 21, 1819-1829.
7. Butt, C.M., Pauly, J.R. & Debski, E.A. (2000) Distribution and development of nicotinic acetylcholine receptor subtypes in the optic tectum of Rana pipiens. J. Comp. Neurol., 423, 603-618.
8. Butt, C.M., Zhao, B., Duncan, M.J. & Debski, E.A. (2002) Sculpting the visual map: the distribution and function of serotonin-1A and serotonin-1B receptors in the optic tectum of the frog. Brain Res., 931, 21-31.
9. Cabelli, R.J., Hohn, A. & Shatz, C.J. (1995) Inhibition of ocular dominance column formation by infusion of NT-4/5 or BDNF. Science, 267, 1662-1666.
10. Cabelli, R.J., Shelton, D.L., Segal, R.A. & Shatz, C.J. (1997) Blockade of endogenous ligands of trkB inhibits formation of ocular dominance columns. Neuron, 19, 63-76.
11. Cauley, K., Agranoff, B.W. & Goldman, D. (1990) Multiple nicotinic acetylcholine receptor genes are expressed in goldfish retina and tectum. J. Neurosci., 10, 670-683.
12. Chavis, P. & Westbrook, G. (2001) Integrins mediate functional pre- and postsynaptic maturation at a hippocampal synapse. Nature, 411, 317-321.
13. Cline, H.T. & Constantine-Paton, M. (1989) NMDA receptor antagonists disrupt the retinotectal topographic map. Neuron, 3, 413-426.
14. Cline, H.T. & Constantine-Paton, M. (1990) NMDA receptor agonist and antagonists alter retinal ganglion cell arbor structure in the developing frog retinotectal projection. J. Neurosci., 10, 1197-1216.
15. Colgin, L.L., Kubota, D. & Lynch, G. (2003) Cholinergic plasticity in the hippocampus. Proc. Natl Acad. Sci. USA, 100, 2872-2877.
16. Conchello, J.A. & Lichtman, J.W. (2005) Optical sectioning microscopy. Nat. Meth., 2, 920-931.
17. DeAngelis, G.C. (2000) Seeing in three dimensions: the neurophysiology of stereopsis. Trends Cogn. Sci., 4, 80-90.
18. Debski, E.A. & Cline, H.T. (2002) Activity-dependent mapping in the retinotectal projection. Curr. Opin. Neurobiol., 12, 93-99.
19. Delibas, N., Doguc, D.K., Sutcu, R., Eroglu, E. & Gokalp, O. (2005) Effect of nicotine on hippocampal nicotinic acetylcholine alpha7 receptor and NMDA receptor subunits 2A and 2B expression in young and old rats. Int. J. Neurosci., 115, 1151-1163.
20. Desan, P.H., Gruberg, E.R., Grewell, K.M. & Eckenstein, F. (1987) Cholinergic innervation of the optic tectum in the frog Rana pipiens. Brain Res., 413, 344-349.
21. Dominguez del Toro, E., Juiz, J.M., Peng, X., Lindstrom, J. & Criado, M. (1994) Immunocytochemical localization of the alpha 7 subunit of the nicotinic acetylcholine receptor in the rat central nervous system. J. Comp. Neurol., 349, 325-342.
22. Edwards, J.A. & Cline, H.T. (1999) Light-induced calcium influx into retinal axons is regulated by presynaptic nicotinic acetylcholine receptor activity in vivo. J. Neurophysiol., 81, 895-907.
23. Feller, M.B. (2002) The role of nAChR-mediated spontaneous retinal activity in visual system development. J. Neurobiol., 53, 556-567.
24. Fenster, C.P., Rains, M.F., Noerager, B., Quick, M.W. & Lester, R.A. (1997) Influence of subunit composition on desensitization of neuronal acetylcholine receptors at low concentrations of nicotine. J. Neurosci., 17, 5747-5759.
25. Foster, A.C. & Wong, E.H. (1987) The novel anticonvulsant MK-801 binds to the activated state of the N-methyl-D-aspartate receptor in rat brain. Br. J. Pharmacol., 91, 403-409.
26. Fried, P.A. & Watkinson, B. (2000) Visuoperceptual functioning differs in 9- to 12-year olds prenatally exposed to cigarettes and marihuana. Neurotoxicol. Teratol., 22, 11-20.
27. Fu, Y., Matta, S.G., James, T.J. & Sharp, B.M. (1998) Nicotine-induced norepinephrine release in the rat amygdala and hippocampus is mediated through brainstem nicotinic cholinergic receptors. J. Pharmacol. Exp. Ther., 284, 1188-1196.
28. 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.
29. Fujii, S., Ji, Z. & Sumikawa, K. (2000) Inactivation of alpha7 ACh receptors and activation of non-alpha7 ACh receptors both contribute to long term potentiation induction in the hippocampal CA1 region. Neurosci. Lett., 286, 134-138.
30. Griesbach, G.S., Hu, D. & Amsel, A. (1998) Effects of MK-801 on vicarious trial-and-error and reversal of olfactory discrimination learning in weanling rats. Behav. Brain Res., 97, 29-38.
31. Grobstein, P., Comer, C., Hollyday, M. & Archer, S.M. (1978) A crossed isthmo-tectal projection in Rana pipiens and its involvement in the ipsilateral visuotectal projection. Brain Res., 156, 117-123.
32. Gruberg, E.R. & Udin, S.B. (1978) Topographic projections between the nucleus isthmi and the tectum of the frog Rana pipiens. J. Comp. Neurol., 179, 487-500.
33. Gruberg, E.R., Wallace, M.T., Caine, H.S. & Mote, M.I. (1991) Behavioral and physiological consequences of unilateral ablation of the nucleus isthmi in the leopard frog. Brain Behav. Evol., 37, 92-103.
34. Henley, J.M., Lindstrom, J.M. & Oswald, R.E. (1986) Acetylcholine receptor synthesis in retina and transport to optic tectum in goldfish. Science, 232, 1627-1629.
35. Hepsen, I.F. & Evereklioglu, C. (2001) Defective visual field tests in chronic heavy smokers. Acta Ophthalmol. Scand., 79, 53-56.
36. Herber, D.L., Severance, E.G., Cuevas, J., Morgan, D. & Gordon, M.N. (2004) Biochemical and histochemical evidence of nonspecific binding of alpha7nAChR antibodies to mouse brain tissue. J. Histochem. Cytochem., 52, 1367-1376.
37. Hernandez, C.M. & Terry, A.V. Jr (2005) Repeated nicotine exposure in rats: effects on memory function, cholinergic markers and nerve growth factor. Neuroscience, 130, 997-1012.
38. Hessler, N.A., Shirke, A.M. & Malinow, R. (1993) The probability of transmitter release at a mammalian central synapse. Nature, 366, 569-572.
39. Horch, H.L. & Sargent, P.B. (1996) Effects of denervation on acetylcholine receptor clusters on frog cardiac ganglion neurons as revealed by quantitative laser scanning confocal microscopy. J. Neurosci., 16, 1720-1729.
40. Huh, G.S., Du Boulanger, L.M.H., Riquelme, P.A., Brotz, T.M. & Shatz, C.J. (2000) Functional requirement for class I MHC in CNS development and plasticity. Science, 290, 2155-2159.
41. Ji, D., Lape, R. & Dani, J.A. (2001) Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity. Neuron, 31, 131-141.
42. Johnston, D., Williams, S., Jaffe, D. & Gray, R. (1992) NMDA-receptor-independent long-term potentiation. Annu. Rev. Physiol., 54, 489-505.
43. King, W.M. (1990) Nicotinic depolarization of optic nerve terminals augments synaptic transmission. Brain Res., 527, 150-154.
44. King, W.M. & Schmidt, J.T. (1991) The long latency component of retinotectal transmission: enhancement by stimulation of nucleus isthmi or tectobulbar tract and block by nicotinic cholinergic antagonists. Neuroscience, 40, 701-712.
45. Krewson, C.E., Dause, R., Mak, M. & Saltzman, W.M. (1996) Stabilization of nerve growth factor in controlled release polymers and in tissue. J. Biomater. Sci. Polym. Ed., 8, 103-117.
46. Levin, E.D., Tizabi, Y., Rezvani, A.H., Caldwell, D.P., Petro, A. & Getachew, B. (2005) Chronic nicotine and dizocilpine effects on regionally specific nicotinic and NMDA glutamate receptor binding. Brain Res., 1041, 132-142.
47. Lindstrom, J., Peng, X., Kuryatov, A., Lee, E., Anand, R., Gerzanich, V.,Wang, F., Wells, G. & Nelson, M. (1998) Molecular and antigenic structure of nicotinic acetylcholine receptors. Ann. NY Acad. Sci., 841, 71-86.
48. Lohmann, T.H., Torrao, A.S., Britto, L.R., Lindstrom, J. & Hamassaki-Britto, D.E. (2000) A comparative non-radioactive in situ hybridization and immunohistochemical study of the distribution of alpha7 and alpha8 subunits of the nicotinic acetylcholine receptors in visual areas of the chick brain. Brain Res., 852, 463-469.
49. Mansvelder, H.D. & McGehee, D.S. (2000) Long-term potentiation of excitatory inputs to brain reward areas by nicotine. Neuron, 27, 349-357.
50. Mansvelder, H.D., van Aerde, K.I., Couey, J.J. & Brussaard, A.B. (2006) Nicotinic modulation of neuronal networks: from receptors to cognition. Psychopharmacology (Berl.), 184, 292-305.
51. Marchi, M., Risso, F., Viola, C., Cavazzani, P. & Raiteri, M. (2002) Direct evidence that release-stimulating alpha7* nicotinic cholinergic receptors are localized on human and rat brain glutamatergic axon terminals. J. Neurochem., 80, 1071-1078.
52. Marín, O. & Gonzalez, A. (1999) Origin of tectal cholinergic projections in amphibians: a combined study of choline acetyltransferase immunohistochemistry and retrograde transport of dextran amines. Vis. Neurosci., 16, 271-283.
53. Marín, O., Smeets, W.J. & Gonzalez, A. (1997) Distribution of choline acetyltransferase immunoreactivity in the brain of anuran (Rana perezi, Xenopus laevis) and urodele (Pleurodeles waltl) amphibians. J. Comp. Neurol., 382, 499-534.
54. 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.
55. McGehee, D.S., Heath, M.J., Gelber, S., Devay, P. & Role, L.W. (1995) Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science, 269, 1692-1696.
56. Min, S.K., Moon, I.W., Ko, R.W. & Shin, H.S. (2001) Effects of transdermal nicotine on attention and memory in healthy elderly non-smokers. Psychopharmacology (Berl.), 159, 83-88.
57. Navalpakkam, V. & Itti, L. (2005) Modeling the influence of task on attention. Vision Res., 45, 205-231.
58. Pakkanen, J.S., Jokitalo, E. & Tuominen, R.K. (2005) Up-regulation of beta2 and alpha7 subunit containing nicotinic acetylcholine receptors in mouse striatum at cellular level. Eur. J. Neurosci., 21, 2681-2691.
59. Prusky, G.T., Shaw, C. & Cynader, M.S. (1988) The distribution and ontogenesis of [3H]nicotine binding sites in cat visual cortex. Brain Res., 467, 161-176.
60. Quick, M.W. & Lester, R.A. (2002) Desensitization of neuronal nicotinic receptors. J. Neurobiol., 53, 457-478.
61. Radcliffe, K.A. & Dani, J.A. (1998) Nicotinic stimulation produces multiple forms of increased glutamatergic synaptic transmission. J. Neurosci., 18, 7075-7083.
62. Ramoa, A.S., Alkondon, M., Aracava, Y., Irons, J., Lunt, G.G., Deshpande, S.S., Wonnacott, S., Aronstam, R.S. & Albuquerque, E.X. (1990) The anticonvulsant MK-801 interacts with peripheral and central nicotinic acetylcholine receptor ion channels. J. Pharmacol. Exp. Ther., 254, 71-82.
63. Reed, B.T., Amthor, F.R. & Keyser, K.T. (2002) Rabbit retinal ganglion cell responses mediated by alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors. Vis. Neurosci., 19, 427-438.
64. Ricciuti, A.J. & Gruberg, E.R. (1985) Nucleus isthmi provides most tectal choline acetyltransferase in the frog Rana pipiens. Brain Res., 341, 399-402.
65. Rizzo, J.F. & 3rd & Lessell, S. (1993) Tobacco amblyopia. Am. J. Ophthalmol., 116, 84-87.
66. Rosenmund, C., Feltz, A. & Westbrook, G.L. (1995) Synaptic NMDA receptor channels have a low open probability. J. Neurosci., 15, 2788-2795.
67. Rossi, F.M., Pizzorusso, T., Porciatti, V., Marubio, L.M., Maffei, L. & Changeux, J.P. (2001) Requirement of the nicotinic acetylcholine receptor beta 2 subunit for the anatomical and functional development of the visual system. Proc. Natl Acad. Sci. USA, 98, 6453-6458.
68. Ruthazer, E.S. & Cline, H.T. (2004) Insights into activity-dependent map formation from the retinotectal system: a middle-of-the-brain perspective. J. Neurobiol., 59, 134-146.
69. Sargent, P.B. (1994) Double-label immunofluorescence with the laser scanning confocal microscope using cyanine dyes. Neuroimage, 1, 288-295.
70. Sargent, P.B., Pike, S.H., Nadel, D.B. & Lindstrom, J.M. (1989) Nicotinic acetylcholine receptor-like molecules in the retina, retinotectal pathway, and optic tectum of the frog. J. Neurosci., 9, 565-573.
71. Schoepfer, R., Conroy, W.G., Whiting, P., Gore, M. & Lindstrom, J. (1990) Brain alpha-bungarotoxin binding protein cDNAs and MAbs reveal subtypes of this branch of the ligand-gated ion channel gene superfamily. Neuron, 5, 35-48.
72. Sedwick, L.A. (1991) The perils of Pauline: visual loss in a tippler. Surv. Ophthalmol., 35, 454-462.
73. Sher, E., Chen, Y., Sharples, T.J., Broad, L.M., Benedetti, G., Zwart, R., McPhie, G.I., Pearson, K.H., Baldwinson, T. & De Filippi, G. (2004) Physiological roles of neuronal nicotinic receptor subtypes: new insights on the nicotinic modulation of neurotransmitter release, synaptic transmission and plasticity. Curr. Top. Med. Chem., 4, 283-297.
74. Shouval, H.Z., Bear, M.F. & Cooper, L.N. (2002) A unified model of NMDA receptor-dependent bidirectional synaptic plasticity. Proc. Natl Acad. Sci. USA, 99, 10831-10836.
75. Silberstein, G.B. & Daniel, C.W. (1982) Elvax 40P implants: sustained, local release of bioactive molecules influencing mammary ductal development. Dev. Biol., 93, 272-278.
76. Smith, A.L., Cordery, P.M. & Thompson, I.D. (1995) Manufacture and release characteristics of Elvax polymers containing glutamate receptor antagonists. J. Neurosci. Meth., 60, 211-217.
77. Swanson, L.W., Simmons, D.M., Whiting, P.J. & Lindstrom, J. (1987) Immunohistochemical localization of neuronal nicotinic receptors in the rodent central nervous system. J. Neurosci., 7, 3334-3342.
78. Takeda, D., Nakatsuka, T., Papke, R. & Gu, J.G. (2003) Modulation of inhibitory synaptic activity by a non-alpha4beta2, non-alpha7 subtype of nicotinic receptors in the substantia gelatinosa of adult rat spinal cord. Pain, 101, 13-23.
79. Taylor, A.C. & Kollros, J.J. (1946) Stages in the normal development of Rana pipiens larvae. Anat. Rec., 94, 7-28.
80. Titmus, M.J., Tsai, H.J., Lima, R. & Udin, S.B. (1999) Effects of choline and other nicotinic agonists on the tectum of juvenile and adult Xenopus frogs: a patch-clamp study. Neuroscience, 91, 753-769.
81. Tu, S., Butt, C.M., Pauly, J.R. & Debski, E.A. (2000) Activity-dependent regulation of substance P expression and topographic map maintenance by a cholinergic pathway. J. Neurosci., 20, 5346-5357.
82. Tu, S. & Debski, E.A. (2001) Neurotrophins, but not depolarization, regulate substance P expression in the developing optic tectum. J. Neurobiol., 48, 131-149.
83. Tzartos, S.J., Rand, D.E., Einarson, B.L. & Lindstrom, J.M. (1981) Mapping of surface structures of electrophorus acetylcholine receptor using monoclonal antibodies. J. Biol. Chem., 256, 8635-8645.
84. Upton, A.L., Ravary, A., Salichon, N., Moessner, R., Lesch, K.P., Hen, R., Seif, I. & Gaspar, P. (2002) Lack of 5-HT (1B) receptor and of serotonin transporter have different effects on the segregation of retinal axons in the lateral geniculate nucleus compared to the superior colliculus. Neuroscience, 111, 597-610.
85. Vallejo, Y.F., Buisson, B., Bertrand, D. & Green, W.N. (2005) Chronic nicotine exposure upregulates nicotinic receptors by a novel mechanism. J. Neurosci., 25, 5563-5572.
86. Vizi, E.S. & Lendvai, B. (1999) Modulatory role of presynaptic nicotinic receptors in synaptic and non-synaptic chemical communication in the central nervous system. Brain Res. Brain Res. Rev., 30, 219-235.
87. Weber, C., Wermter, S. & Elshaw, M. (2005) A hybrid generative and predictive model of the motor cortex. Neural Netw., 19, 339-353.
88. Wong, E.H., Kemp, J.A., Priestley, T., Knight, A.R.,Woodruff, G.N. & Iversen, L.L. (1986) The anticonvulsant MK-801 is a potent N-methyl-D-aspartate antagonist. Proc. Natl Acad. Sci. USA, 83, 7104-7108.
89. Wu, H.H., Cork, R.J. & Mize, R.R. (2000) Normal development of the ipsilateral retinocollicular pathway and its disruption in double endothelial and neuronal nitric oxide synthase gene knockout mice. J. Comp. Neurol., 426, 651-665.
90. Wu, H.H., Selski, D.J., El-Fakahany, E.E. & McLoon, S.C. (2001) The role of nitric oxide in development of topographic precision in the retinotectal projection of chick. J. Neurosci., 21, 4318-4325.
91. 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.
92. Yu, C.J., Butt, C.M. & Debski, E.A. (2003) Bidirectional modulation of visual plasticity by cholinergic receptor subtypes in the frog optic tectum. Eur. J. Neurosci., 17, 1253-1265.
93. Yu, C.J. & Debski, E.A. (2003) The effects of nicotinic and muscarinic receptor activation on patch-clamped cells in the optic tectum of Rana pipiens. Neuroscience, 118, 135-144.