Nicotine exposure during adolescence alters the rules for prefrontal cortical synaptic plasticity during adulthood

Frontiers in Synaptic Neuroscience

Volumn , Issue AUGUST, 2012, Pages

  Goriounova, Natalia A ^a   Mansvelder, Huibert D ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

Adolescence; Cognitive behavior; Mglur; Nachr; Nicotine; Prefrontal cortex; Stdp

Indexed keywords

METABOTROPIC RECEPTOR; NICOTINE;

ADOLESCENT; ARTICLE; ATTENTION; CIGARETTE SMOKING; COGNITIVE DEFECT; ENVIRONMENTAL EXPOSURE; EXECUTIVE FUNCTION; GABAERGIC SYSTEM; HUMAN; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PREFRONTAL CORTEX; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SYNAPSE; UPREGULATION;

EID: 84866041673     PISSN: None     EISSN: 16633563     Source Type: Journal    
DOI: 10.3389/fnsyn.2012.00003     Document Type: Article

References (106)

1. Abreu-Villaca, Y., Seidler, F. J., Qiao, D.,Tate,C.A.,Cousins,M.M., Thillai, I., and Slotkin, T. A. (2003). Short-term adolescent nicotine exposure has immediate and persistent effects on cholinergic systems: critical periods, patterns of exposure, dose thresholds. Neuropsychopharmacology 28, 1935-1949.
2. Adriani, W., Spijker, S., DerocheGamonet,V.,Laviola,G.,LeMoal, M., Smit, A. B., and Piazza, P. V. (2003). Evidence for enhanced neurobehavioral vulnerability to nicotine during periadolescence in rats. J. Neurosci. 23, 4712-4716.
3. Alkondon, M., and Albuquerque, E. X. (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, E. F., Eisenberg, H. M., and Albuquerque, E. X. (2000). Nicotinic receptor activation in human cerebral cortical interneurons: a mechanism for inhibition and disinhibition of neuronal networks. J. Neurosci. 20, 66-75.
5. Belluzzi, J. D., Lee, A. G., Oliff, H. S., and Leslie, F. M. (2004). Agedependent effects of nicotine on locomotor activity and conditioned place preference in rats. Psychopharmacology (Berl.) 174, 389-395.
6. Bergstrom, H. C., McDonald, C. G., French, H. T., and Smith, R. F. (2008). Continuous nicotine administration produces selective, age-dependent structural alteration of pyramidal neurons from prelimbic cortex. Synapse 62, 31-39.
7. Bi, G., and Poo, M. (2001). Synaptic modification by correlated activity: Hebb's postulate revisited. Annu. Rev. Neurosci. 24, 139-166.
8. Bradley, S. R., Marino, M. J., Wittmann, M.,Rouse,S.T.,Awad,H.,Levey, A. I., and Conn, P. J. (2000). Activation of group II metabotropic glutamate receptors inhibits synaptic excitation of the substantia Nigra pars reticulata. J. Neurosci. 20, 3085-3094.
9. Brielmaier,J.M.,McDonald,C.G., and Smith, R. F. (2007). Immediate and long-term behavioral effects of a single nicotine injection in adolescent and adult rats. Neurotoxicol. Teratol. 29, 74-80.
10. Brook, J. S., Schuster, E., and Zhang, C. (2004). Cigarette smoking and depressive symptoms: a longitudinal study of adolescents and young adults. Psychol. Rep. 95, 159-166.
11. Brown, R. A., Lewinsohn, P. M., Seeley, J. R., and Wagner, E. F. (1996). Cigarette smoking, major depression, and other psychiatric disorders among adolescents. J. Am. Acad. Child Adolesc. Psychiatry 35, 1602-1610.
12. Brown, R. W., and Kolb, B. (2001). Nicotine sensitization increases dendritic length and spine density in the nucleus accumbens and cingulate cortex. Brain Res. 899, 94-100.
13. Brunzell, D. H., Russell, D. S., and Picciotto, M. R. (2003). In vivo nicotine treatment regulates mesocorticolimbic CREB and ERK signaling in C57Bl/6J mice. J. Neurochem. 84, 1431-1441.
14. Casey, B. J., Tottenham, N., Liston, C., and Durston, S. (2005). Imaging the developing brain: what have we learned about cognitive development? Trends Cogn. Sci. 9, 104-110.
15. Cervilla,J.A.,Prince,M.,andMann, A. (2000). Smoking, drinking, and incident cognitive impairment: a cohort community based study included in the Gospel Oak project. J. Neurol. Neurosurg. Psychiatry 68, 622-626.
16. Choi,W.S.,Patten,C.A.,Gillin,J. C.,Kaplan,R.M.,andPierce,J.P. (1997). Cigarette smoking predicts development of depressive symptoms among U.S. adolescents. Ann. Behav. Med. 19, 42-50.
17. Chung, S., Li, X., and Nelson, S. B. (2002). Short-term depression at thalamocortical synapses contributes to rapid adaptation of cortical sensory responses in vivo. Neuron 34, 437-446.
18. Conn, P. J., Lindsley, C. W., and Jones, C. K. (2009). Activation of metabotropic glutamate receptors as a novel approach for the treatment of schizophrenia. Trends Pharmacol. Sci. 30, 25-31.
19. Couey, J. J., Meredith, R. M., Spijker, S., Poorthuis, R. B., Smit, A. B., Brussaard, A. B., and Mansvelder, H. D. (2007). Distributed network actions by nicotine increase the threshold for spike-timing-dependent plasticity in prefrontal cortex. Neuron 54, 73-87.
20. Counotte, D. S., Goriounova, N. A., Li, K. W., Loos, M., van der Schors, R. C., Schetters, D., Schoffelmeer, A. N. M., Smit, A. B., Mansvelder, H. D., Pattij, T., and Spijker, S. (2011). Lasting synaptic changes underlie attention deficits caused by nicotine exposure during adolescence. Nat. Neurosci. 14, 417-419.
21. Counotte, D. S., Goriounova, N. A., Moretti, M., Smoluch, M. T., Irth, H.,Clementi,F.,Schoffelmeer,A. N. M., Mansvelder, H. D., Smit, A. B., Gotti, C., and Spijker, S. (2012). Adolescent nicotine exposure transiently increases high-affinity nicotinic receptors and modulates inhibitory synaptic transmission in rat medial prefrontal cortex. FASEB J. 26, 810-820.
22. Counotte, D. S., Spijker, S., van de Burgwal, L. H., Hogenboom, F., Schoffelmeer, A. N., De Vries, T. J., Smit, A. B., and Pattij, T. (2009). Long-lasting cognitive deficits resulting from adolescent nicotine exposure in rats. Neuropsychopharmacology 34, 299-306.
23. Cruz, D. A., Eggan, S. M., and Lewis, D. A. (2003). Postnatal development of preand postsynaptic GABA markers at chandelier cell connections with pyramidal neurons in monkey prefrontal cortex. J. Comp. Neurol. 465, 385-400.
24. Currie, C. N. G. S., Godeau, E., Roberts, C.,Smith,R.,Currie,D.,Pickett,W., Richter, M., Morgan, A., Barnekow, V. (2008). " Inequalities in young people's health (1993). HBSC international report from the 2005/06 Survey," in Health Policy for Children and Adolescents, No. 5.edC.Currie (Kopenhagen: WHO Regional Office for Europe).
25. Dani, J. A., and Bertrand, D. (2007). Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. Annu. Rev. Pharmacol. Toxicol. 47, 699-729.
26. Deas, D. (2006). Adolescent substance abuse and psychiatric comorbidities. J. Clin. Psychiatry 67(Suppl. 7), 18-23.
27. Doura, M. B., Gold, A. B., Keller, A. B., and Perry, D. C. (2008). Adult and periadolescent rats differ in expression of nicotinic cholinergic receptor subtypes and in the response of these subtypes to chronic nicotine exposure. Brain Res. 1215, 40-52.
28. Feldman, D. E., and Brecht, M. (2005). Map plasticity in somatosensory cortex. Science 310, 810-815.
29. Feldman, D. E., Nicoll, R. A., and Malenka, R. C. (1999). Synaptic plasticity at thalamocortical synapses in developing rat somatosensory cortex: LTP, LTD, and silent synapses. J. Neurobiol. 41, 92-101.
30. Floresco, S. B., Braaksma, D. N., and Phillips, A. G. (1999). Thalamiccortical-striatal circuitry subserves working memory during delayed responding on a radial arm maze. J. Neurosci. 19,11061-11071.
31. Fountain, S. B., Rowan, J. D., Kelley, B. M., Willey, A. R., and Nolley, E. P. (2008). Adolescent exposure to nicotine impairs adult serial pattern learning in rats. Exp. Brain Res. 187, 651-656.
32. Fu, X. W., Lindstrom, J., and Spindel, E. R. (2009). Nicotine activates and up-regulates nicotinic acetylcholine receptors in bronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 41, 93-99.
33. Galvan,A.,Hare,T.,Voss,H.,Glover, G., and Casey, B. J. (2007). Risktaking and the adolescent brain: whoisatrisk?Dev. Sci. 10, F8-F14.
34. Giedd, J. N. (2004). Structural magnetic resonance imaging of the adolescent brain. Ann. N.Y. Acad. Sci. 1021, 77-85.
35. Gioanni, Y., Rougeot, C., Clarke, P. B., Lepouse, C., Thierry, A. M., and Vidal, C. (1999). Nicotinic receptors in the rat prefrontal cortex: increase in glutamate release and facilitation of mediodorsal thalamo-cortical transmission. Eur. J. Neurosci. 11, 18-30.
36. Gogtay, N., Giedd, J. N., Lusk, L., Hayashi, K. M., Greenstein, D., Vaituzis,A.C.,Nugent,T.F.3rd., Herman, D. H., Clasen, L. S., Toga, A. W., Rapoport, J. L., and Thompson, P. M. (2004). Dynamic mapping of human cortical development during childhood through early adulthood. Proc. Natl. Acad. Sci. U.S.A. 101, 8174-8179.
37. Goriounova, N. A., and Mansvelder, H. D. (2012). Nicotine exposure during adolescence leads to shortand long-term changes in spiketiming-dependent plasticity in rat prefrontal cortex. J. Neurosci. [Epub ahead of print].
38. Govind, A. P., Vezina, P., and Green, W. N. (2009). Nicotine-induced upregulation of nicotinic receptors: underlying mechanisms and relevance to nicotine addiction. Biochem. Pharmacol. 78, 756-765.
39. Grady, S. R., Murphy, K. L., Cao, J.,Marks,M.J.,McIntosh,J. M., and Collins, A. C. (2002). Characterization of nicotinic agonist-induced [H-3] dopamine release from synaptosomes prepared from four mouse brain regions. J. Pharmacol. Exp. Ther. 301, 651-660.
40. Grunbaum, J. A., Kann, L., Kinchen, S.,Ross,J.,Hawkins,J.,Lowry,R., Harris,W.A.,McManus,T.,Chyen, D., and Collins, J. (2004). Youth risk behavior surveillance-United States (2003). MMWR Surveill. Summ. 53, 1-96.
41. Guillem, K., Bloem, B., Poorthuis, R. B.,Loos,M.,Smit,A.B.,Maskos, U., Spijker, S., and Mansvelder, H. D. (2011). Nicotinic acetylcholine receptor beta2 subunits in the medial prefrontal cortex control attention. Science 333, 888-891.
42. Gulledge, A. T., Park, S. B., Kawaguchi, Y., and Stuart, G. J. (2007). Heterogeneity of phasic cholinergic signaling in neocortical neurons. J. Neurophysiol. 97, 2215-2229.
43. Gupta, D. S., McCullumsmith, R. E., Beneyto, M., Haroutunian, V., Davis, K. L., and Meador-Woodruff, J. H. (2005). Metabotropic glutamate receptor protein expression in the prefrontal cortex and striatum in schizophrenia. Synapse 57, 123-131.
44. Hebb, D. (1949). The Organization of Behaviour. New York: John Wiley.
45. Helton, D. R., Tizzano, J. P., Monn, J. A., Schoepp, D. D., and Kallman, M. J. (1997). LY354740, a metabotropic glutamate receptor agonist which ameliorates symptoms of nicotine withdrawal in rats. Neuropharmacology 36, 1511-1516.
46. Iniguez, S. D., Warren, B. L., Parise, E. M., Alcantara, L. F., Schuh, B., Maffeo, M. L., Manojlovic, Z., and Bolanos-Guzman, C. A. (2008). Nicotine exposure during adolescence induces a depression-like state in adulthood. Neuropsychopharmacology 34, 1609-1624.
47. Jacobsen, L. K., Krystal, J. H., Mencl, W. E., Westerveld, M., Frost, S. J., and Pugh, K. R. (2005). Effects of smoking and smoking abstinence on cognition in adolescent tobacco smokers. Biol. Psychiatry 57, 56-66.
48. Jacobsen, L. K., Mencl, W. E., Constable, R. T., Westerveld, M., and Pugh, K. R. (2007). Impact of smoking abstinence on working memory neurocircuitry in adolescent daily tobacco smokers. Psychopharmacology (Berl.) 193, 557-566.
49. Jay, T. M., and Witter, M. P. (1991). Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin. J. Comp. Neurol. 313, 574-586.
50. Ji, D., and Dani, J. A. (2000). Inhibition and disinhibition of pyramidal neurons by activation of nicotinic receptors on hippocampal interneurons. J. Neurophysiol. 83, 2682-2690.
51. Jones, S., and Yakel, J. L. (1997). Functional nicotinic ACh receptors on interneurones in the rat hippocampus. J. Physiol. 504(Pt 3), 603-610.
52. Kalmijn, S., van Boxtel, M. P., Verschuren, M. W., Jolles, J., and Launer, L. J. (2002). Cigarette smoking and alcohol consumption in relation to cognitive performance in middle age. Am. J. Epidemiol. 156, 936-944.
53. Kapfer, C., Glickfeld, L. L., Atallah, B. V., and Scanziani, M. (2007). Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat. Neurosci. 10, 743-753.
54. Kawaguchi, Y. (1993). Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. J. Neurophysiol. 69, 416-431.
55. Kawaguchi, Y., and Kondo, S. (2002). Parvalbumin, somatostatin and cholecystokinin as chemical markers for specific GABAergic interneuron types in the rat frontal cortex. J. Neurocytol. 31, 277-287.
56. Kawaguchi, Y., and Kubota, Y. (1997). GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex 7, 476-486.
57. Kenny, P. J., Gasparini, F., and Markou, A. (2003). Group II metabotropic and alpha-amino-3-hydroxy-5methyl-4-isoxazole propionate (AMPA)/kainate glutamate receptors regulate the deficit in brain reward function associated with nicotine withdrawal in rats. J. Pharmacol. Exp. Ther. 306, 1068-1076.
58. Kenny, P. J., and Markou, A. (2004). The ups and downs of addiction: role of metabotropic glutamate receptors. Trends Pharmacol. Sci. 25, 265-272.
59. Kota, D., Robinson, S. E., and Imad Damaj, M. (2009). Enhanced nicotine reward in adulthood after exposure to nicotine during early adolescence in mice. Biochem. Pharmacol. 78, 873-879.
60. O'Dell, L. E. (2009). A psychobiological framework of the substrates that mediate nicotine use during adolescence. Neuropharmacology 56(Suppl. 1), 263-278.
61. Lambe, E. K., Picciotto, M. R., and Aghajanian, G. K. (2003). Nicotine induces glutamate release from thalamocortical terminals in prefrontal cortex. Neuropsychopharmacology 28, 216-225.
62. Le Novere, N., Corringer, P. J., and Changeux, J. P. (2002). The diversity of subunit composition in nAChRs: evolutionary origins, physiologic and pharmacologic consequences. J. Neurobiol. 53, 447-456.
63. Lester, H. A., Xiao, C., Srinivasan, R.,Son,C.D.,Miwa,J.,Pantoja, R., Banghart, M. R., Dougherty, D.A.,Goate,A.M.,andWang,J. C. (2009). Nicotine is a selective pharmacological chaperone of acetylcholine receptor number and stoichiometry. Implications for drug discovery. AAPS J. 11, 167-177.
64. Letzkus, J. J., Kampa, B. M., and Stuart, G. J. (2007). Does spike timing-dependent synaptic plasticity underlie memory formation? Clin.Exp.Pharmacol.Physiol.34, 1070-1076.
65. Liechti, M. E., Lhuillier, L., Kaupmann, K., and Markou, A. (2007). Metabotropic glutamate 2/3 receptors in the ventral tegmental area and the nucleus accumbens shell are involved in behaviors relating to nicotine dependence. J. Neurosci. 27, 9077-9085.
66. Mansvelder, H. D., Keath, J. R., and McGehee, D. S. (2002). Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas. Neuron 33, 905-919.
67. Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., and Wu, C. (2004). Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 5, 793-807.
68. Marks, M. J., McClure-Begley, T. D., Whiteaker, P., Salminen, O., Brown, R. W., Cooper, J., Collins, A. C., and Lindstrom, J. M. (2011). Increased nicotinic acetylcholine receptor protein underlies chronic nicotine-induced up-regulation of nicotinic agonist binding sites in mouse brain. J. Pharmacol. Exp. Ther. 337, 187-200.
69. Marks, M. J., Pauly, J. R., Gross, S. D., Deneris, E. S., Hermans-Borgmeyer, I., Heinemann, S. F., and Collins, A. C. (1992). Nicotine binding and nicotinic receptor subunit RNA after chronic nicotine treatment. J. Neurosci. 12, 2765-2784.
70. Mateo, Z., and Porter, J. T. (2007). Group II metabotropic glutamate receptors inhibit glutamate release at thalamocortical synapses in the developing somatosensory cortex. Neuroscience 146, 1062-1072.
71. McGehee, D. S. (2002). Nicotinic receptors and hippocampal synaptic plasticity. it's all in the timing. Trends Neurosci. 25, 171.
72. McGehee, D. S., and Role, L. W. (1995). Physiological diversity of nicotinic acetylcholine receptors expressed by vertebrate neurons. Annu. Rev. Physiol. 57, 521-546.
73. McQuiston, A. R., and Madison, D. V. (1999). Nicotinic receptor activation excites distinct subtypes of interneurons in the rat hippocampus. J. Neurosci. 19, 2887-2896.
74. Melendez, R. I., Gregory, M. L., Bardo, M. T., and Kalivas, P. W. (2004). Impoverished rearing environment alters metabotropic glutamate receptor expression and function in the prefrontal cortex. Neuropsychopharmacology 29, 1980-1987.
75. Millar, N. S., and Gotti, C. (2009). Diversity of vertebrate nicotinic acetylcholine receptors. Neuropharmacology 56, 237-246.
76. Mineur,Y.S.,andPicciotto,M.R. (2008). Genetics of nicotinic acetylcholine receptors: relevance to nicotine addiction. Biochem. Pharmacol. 75, 323-333.
77. Miwa,J.M.,Freedman,R.,andLester, H. A. (2011). Neural systems governed by nicotinic acetylcholine receptors: emerging hypotheses. Neuron 70, 20-33.
78. Musso, F., Bettermann, F., Vucurevic, G., Stoeter, P., Konrad, A., and Winterer, G. (2007). Smoking impacts on prefrontal attentional network function in young adult brains. Psychopharmacology (Berl.) 191, 159-169.
79. Orr, D. P., and Ingersoll, G. M. (1995). The contribution of level of cognitive complexity and pubertal timing to behavioral risk in young adolescents. Pediatrics 95, 528-533.
80. Palucha, A., and Pilc, A. (2005). The involvement of glutamate in the pathophysiology of depression. Drug News Perspect. 18, 262-268.
81. Peto, R.,Chen, Z.M.,and Boreham, J. (1999). Tobacco-the growing epidemic. Nat. Med. 5, 15-17.
82. Pilc, A., Chaki, S., Nowak, G., and Witkin, J. M. (2008). Mood disorders: regulation by metabotropic glutamate receptors. Biochem. Pharmacol. 75, 997-1006.
83. Polesskaya, O. O., Fryxell, K. J., Merchant,A.D.,Locklear,L.L.,Ker, K. F., McDonald, C. G., Eppolito, A. K., Smith, L. N., Wheeler, T. L., and Smith, R. F. (2007). Nicotine causes age-dependent changes in gene expression in the adolescent female rat brain. Neurotoxicol. Teratol. 29, 126-140.
84. Poorthuis, R. B., Bloem, B., Schak, B., Wester, J., de Kock, C. P. J., and Mansvelder, H. D. (2012). Layerspecific modulation of the prefrontal cortex by nicotinic acetylcholine receptors. Cereb. Cortex. [Epub ahead of print].
85. Poorthuis, R. B., Goriounova, N. A., Couey, J. J., and Mansvelder, H. D. (2009). Nicotinic actions on neuronal networks for cognition: general principles and long-term consequences. Biochem. Pharmacol. 78, 668-676.
86. Portugal, G. S., Wilkinson, D. S., Turner, J. R., Blendy, J. A., and Gould T. J. (2012). Developmental effects of acute, chronic, and withdrawal from chronic nicotine on fear conditioning. Neurobiol. Learn. Mem. 97, 482-494.
87. Pozzi, L., Baviera, M., Sacchetti, G.,Calcagno,E.,Balducci,C., Invernizzi,R.W.,andCarli,M. (2011). Attention deficit induced by blockade of N-methyl d-aspartate receptors in the prefrontal cortex is associated with enhanced glutamate release and cAMP response element binding protein phosphorylation: role of metabotropic glutamate receptors 2/3. Neuroscience 176, 336-348.
88. Richards, M., Jarvis, M. J., Thompson, N., and Wadsworth, M. E. (2003). Cigarette smoking and cognitive decline in midlife: evidence from a prospective birth cohort study. Am. J. Public Health 93, 994-998.
89. Schochet, T. L., Bremer, Q. Z., Brownfield, M. S., Kelley, A. E., and Landry, C. F. (2008). The dendritically targeted protein Dendrin is induced by acute nicotine in cortical regions of adolescent rat brain. Eur. J. Neurosci. 28, 1967-1979.
90. Schochet, T. L., Kelley, A. E., and Landry, C. F. (2005). Differential expression of arc mRNA and other plasticity-related genes induced by nicotine in adolescent rat forebrain. Neuroscience 135, 285-297.
91. Shram, M. J., Funk, D., Li, Z., and Le, A. D. (2006). Periadolescent and adult rats respond differently in tests measuring the rewarding and aversive effects of nicotine. Psychopharmacology (Berl.) 186, 201-208.
92. Silberberg, G., and Markram, H. (2007). Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53, 735-746.
93. Song, S., and Abbott, L. F. (2001). Cortical development and remapping through spike timingdependent plasticity. Neuron 32, 339-350.
94. Sowell, E. R., Peterson, B. S., Thompson, P. M., Welcome, S. E., Henkenius, A. L., and Toga, A. W. (2003). Mapping cortical change across the human life span. Nat. Neurosci. 6, 309-315.
95. Sowell, E. R., Thompson, P. M., Leonard,C.M.,Welcome,S.E., Kan, E., and Toga, A. W. (2004). Longitudinal mapping of cortical thickness and brain growth in normal children. J. Neurosci. 24, 8223-8231.
96. Spear, L. P. (2000). The adolescent brain and age-related behavioral manifestations. Neurosci. Biobehav. Rev. 24, 417-463.
97. Takahashi, T., Forsythe, I. D., Tsujimoto, T., Barnes-Davies, M., and Onodera, K. (1996). Presynaptic calcium current modulation by a metabotropic glutamate receptor. Science 274, 594-597.
98. Tierney, P. L., Degenetais, E., Thierry, A. M., Glowinski, J., and Gioanni, Y. (2004). Influence of the hippocampus on interneurons of the rat prefrontal cortex. Eur. J. Neurosci. 20, 514-524.
99. Trauth, J. A., Seidler, F. J., and Slotkin, T. A. (2000). An animal model of adolescent nicotine exposure: effects on gene expression and macromolecular constituents in rat brain regions. Brain Res. 867, 29-39.
100. Vastola, B. J., Douglas, L. A., Varlinskaya, E. I., and Spear, L. P. (2002). Nicotine-induced conditioned place preference in adolescent and adult rats. Physiol. Behav. 77, 107-114.
101. Wonnacott, S. (1990). The paradox of nicotinic acetylcholine receptor upregulation by nicotine. Trends Pharmacol. Sci. 11, 216-219.
102. Wonnacott, S., Sidhpura, N., and Balfour, D. J. K. (2005). Nicotine from molecular mechanisms to behaviour. Curr. Opin. Pharmacol. 5, 53.
103. Woo,T.U.,Pucak,M.L.,Kye,C. H., Matus, C. V., and Lewis, D. A. (1997). Peripubertal refinement of the intrinsic and associational circuitry in monkey prefrontal cortex. Neuroscience 80, 1149-1158.
104. Xiang, Z., Huguenard, J. R., and Prince, D. A. (1998). Cholinergic switching within neocortical inhibitory networks. Science 281, 985-988.
105. Zucker, R. S. (1989). Short-term synaptic plasticity. Annu. Rev. Neurosci. 12, 13-31.
106. Zucker, R. S., and Regehr, W. G. (2002). Short-term synaptic plasticity. Annu. Rev. Physiol. 64, 355-405.