Acute nicotine administration increases BOLD fMRI signal in brain regions involved in reward signaling and compulsive drug intake in rats

International Journal of Neuropsychopharmacology

Volumn 18, Issue 2, 2015, Pages 1-13

  Bruijnzeel, Adrie W ^a   Alexander, Jon C ^a   Perez, Pablo D ^a   Bauzo Rodriguez, Rayna ^a   Hall, Gabrielle ^a   Klausner, Rachel ^a   Guerra, Valerie ^a   Zeng, Huadong ^b   Igari, Moe ^a   Febo, Marcelo ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

addiction; compulsive behavior; nicotine; pharmacological fMRI; rats; reward

Indexed keywords

MECAMYLAMINE; NICOTINE; NICOTINIC AGENT; NICOTINIC RECEPTOR BLOCKING AGENT; OXYGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BOLD SIGNAL; BRAIN REGION; COGNITION; COMPARATIVE STUDY; COMPULSION; CONTROLLED STUDY; DRUG EFFECT; ELECTROENCEPHALOGRAM; FUNCTIONAL MAGNETIC RESONANCE IMAGING; IMAGE PROCESSING; IMAGE RECONSTRUCTION; INSULA; MALE; MOTOR PERFORMANCE; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; NUCLEUS ACCUMBENS SHELL; PRIORITY JOURNAL; RAT; REWARD; SIGNAL TRANSDUCTION; ANIMAL; BLOOD; BRAIN; BRAIN CIRCULATION; BRAIN MAPPING; DOSE RESPONSE; DRUG EFFECTS; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; WISTAR RAT;

ANIMALS; BRAIN; BRAIN MAPPING; CEREBROVASCULAR CIRCULATION; COMPULSIVE BEHAVIOR; DOSE-RESPONSE RELATIONSHIP, DRUG; MAGNETIC RESONANCE IMAGING; MALE; MECAMYLAMINE; NICOTINE; NICOTINIC AGONISTS; NICOTINIC ANTAGONISTS; OXYGEN; RATS, WISTAR; REWARD;

EID: 84931268772     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1093/ijnp/pyu011     Document Type: Article

References (81)

1. Balleine BW, Killcross S (2006) Parallel incentive processing: an integrated view of amygdala function. Trends Neurosci 29:272-279.
2. Baxter LR, Jr., Phelps ME, Mazziotta JC, Guze BH, Schwartz JM, Selin CE (1987) Local cerebral glucose metabolic rates in obsessive-compulsive disorder. A comparison with rates in unipolar depression and in normal controls. Arch Gen Psychiatry 44:211-218.
3. Benowitz NL (1988) Drug therapy. Pharmacologic aspects of cigarette smoking and nicotine addition. N Engl J Med 319:1318-1330.
4. Bruijnzeel AW (2012) Tobacco addiction and the dysregulation of brain stress systems. Neurosci Biobehav Rev 36:1418-1441.
5. Bruijnzeel AW, Zislis G, Wilson C, Gold MS (2007) Antagonism of CRF receptors prevents the deficit in brain reward function associated with precipitated nicotine withdrawal in rats. Neuropsychopharmacology 32:955-963.
6. Brunzell DH, Boschen KE, Hendrick ES, Beardsley PM, McIntosh JM (2010) Alpha-conotoxin MII-sensitive nicotinic acetylcholine receptors in the nucleus accumbens shell regulate progressive ratio responding maintained by nicotine. Neuropsychopharmacology 35:665-673.
7. Cai YQ, Wang W, Hou YY, Zhang Z, Xie J, Pan ZZ (2013) Central amygdala GluA1 facilitates associative learning of opioid reward. J Neurosci 33:1577-1588.
8. Cheeta S, Irvine E, File SE (2001) Social isolation modifies nicotines effects in animal tests of anxiety. Br J Pharmacol 132:1389-1395.
9. Elliott BM, Faraday MM, Phillips JM, Grunberg NE (2004) Effects of nicotine on elevated plus maze and locomotor activity in male and female adolescent and adult rats. Pharmacol Biochem Behav 77:21-28.
10. Everitt BJ, Robbins TW (2005) Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 8:1481-1489.
11. Everitt BJ, Morris KA, OBrien A, Robbins TW (1991) The basolateral amygdala-ventral striatal system and conditioned place preference: further evidence of limbic-striatal interactions underlying reward-related processes. Neuroscience 42:1-18.
12. Febo M (2011) Technical and conceptual considerations for performing and interpreting functional MRI studies in awake rats. Front Psychiatry 2:43. doi: 10.3389/fpsyt.2011.00043.
13. Fehr C, Yakushev I, Hohmann N, Buchholz HG, Landvogt C, Deckers H, Eberhardt A, Klager M, Smolka MN, Scheurich A, Dielentheis T, Schmidt LG, Rosch F, Bartenstein P, Grunder G, Schreckenberger M (2008) Association of low striatal dopamine d2 receptor availability with nicotine dependence similar to that seen with other drugs of abuse. Am J Psychiatry 165:507-514.
14. Ferris CF, Kulkarni P, Sullivan JM, Jr., Harder JA, Messenger TL, Febo M (2005) Pup suckling is more rewarding than cocaine: evidence from functional magnetic resonance imaging and three-dimensional computational analysis. J Neurosci 25:149-156.
15. Ferris CF, Febo M, Luo F, Schmidt K, Brevard M, Harder JA, Kulkarni P, Messenger T, King JA (2006) Functional magnetic resonance imaging in conscious animals: a new tool in behavioural neuroscience research. J Neuroendocrinol 18:307-318.
16. Fowler CD, Kenny PJ (2014) Nicotine aversion: Neurobiological mechanisms and relevance to tobacco dependence vulnerability. Neuropharmacology 76:533-544.
17. Fowler CD, Lu Q, Johnson PM, Marks MJ, Kenny PJ (2011) Habenular alpha5 nicotinic receptor subunit signalling controls nicotine intake. Nature 471:597-601.
18. Fowler CD, Tuesta L, Kenny PJ (2013) Role of alpha5nicotinic acetylcholine receptors in the effects of acute and chronic nicotine treatment on brain reward function in mice. Psychopharmacology (Berl) 229:503-513.
19. Franklin TR, Wang Z, Wang J, Sciortino N, Harper D, Li Y, Ehrman R, Kampman K, OBrien CP, Detre JA, Childress AR (2007) Limbic activation to cigarette smoking cues independent of nicotine withdrawal: a perfusion fMRI study. Neuropsychopharmacology 32:2301-2309.
20. Fuchs RA, Evans KA, Ledford CC, Parker MP, Case JM, Mehta RH, See RE (2005) The role of the dorsomedial prefrontal cortex, basolateral amygdala, and dorsal hippocampus in contextual reinstatement of cocaine seeking in rats. Neuropsychopharmacology 30:296-309.
21. Genovese CR, Lazar NA, Nichols T (2002) Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15:870-878.
22. Gozzi A, Schwarz A, Reese T, Bertani S, Crestan V, Bifone A (2006) Region-specific effects of nicotine on brain activity: a pharmacological MRI study in the drug-naive rat. Neuropsychopharmacology 31:1690-1703.
23. Grabenhorst F, Hernadi I, Schultz W (2012) Prediction of economic choice by primate amygdala neurons. Proc Natl Acad Sci USA 109:18950-18955.
24. Hashemizadeh S, Sardari M, Rezayof A (2014) Basolateral amygdala CB1 cannabinoid receptors mediate nicotine-induced place preference. Prog Neuropsychopharmacol Biol Psychiatry 51C:65-71.
25. Heeger DJ, Ress D (2002) What does fMRI tell us about neuronal activity? Nat Rev Neurosci 3:142-151.
26. Hollander JA, Lu Q, Cameron MD, Kamenecka TM, Kenny PJ (2008) Insular hypocretin transmission regulates nicotine reward. Proc Natl Acad Sci USA 105:19480-19485.
27. Horan JJ, Linberg SE, Hackett G (1977) Nicotine poisoning and rapid smoking. J Consult Clin Psychol 45:344-347.
28. Hurd YL, Suzuki M, Sedvall GC (2001) D1 and D2 dopamine receptor mRNA expression in whole hemisphere sections of the human brain. J Chem Neuroanat 22:127-137.
29. Igari M, Alexander JC, Ji Y, Qi X, Papke RL, Bruijnzeel AW (2013) Varenicline and cytisine diminish the dysphoric-like state associated with spontaneous nicotine withdrawal in rats. Neuropsychopharmacology 39:455-465.
30. Ikemoto S (2007) Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbensolfactory tubercle complex. Brain Res Rev 56:27-78.
31. Jackson KJ, Sanjakdar SS, Muldoon PP, McIntosh JM, Damaj MI (2013) The alpha3beta4nicotinic acetylcholine receptor subtype mediates nicotine reward and physical nicotine withdrawal signs independently of the alpha5 subunit in the mouse. Neuropharmacology 70:228-235.
32. Janes AC, Pizzagalli DA, Richardt S, Frederick BD, Chuzi S, Pachas G, Culhane MA, Holmes AJ, Fava M, Evins AE, Kaufman MJ (2010) Brain Reactivity to Smoking Cues Prior to Smoking Cessation Predicts Ability to Maintain Tobacco Abstinence. Biol Psychiatry 67:722-729.
33. Knapska E, Lioudyno V, Kiryk A, Mikosz M, Gorkiewicz T, Michaluk P, Gawlak M, Chaturvedi M, Mochol G, Balcerzyk M, Wojcik DK, Wilczynski GM, Kaczmarek L (2013) Reward learning requires activity of matrix metalloproteinase-9 in the central amygdala. J Neurosci 33:14591-14600.
34. Koob GF, Volkow ND (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35:217-238.
35. Kutlu MG, Burke D, Slade S, Hall BJ, Rose JE, Levin ED (2013) Role of insular cortex D(1) and D(2) dopamine receptors in nicotine self-administration in rats. Behav Brain Res 256:273-278.
36. Laviolette SR, van der Kooy D (2003) The motivational valence of nicotine in the rat ventral tegmental area is switched from rewarding to aversive following blockade of the alpha7-subunit- containing nicotinic acetylcholine receptor. Psychopharmacology (Berl) 166:306-313.
37. Le Foll B, Goldberg SR (2005) Nicotine induces conditioned place preferences over a large range of doses in rats. Psychopharmacology (Berl) 178:481-492.
38. Li Z, DiFranza JR, Wellman RJ, Kulkarni P, King JA (2008) Imaging brain activation in nicotine-sensitized rats. Brain Res 1199:91-99.
39. Liu L, Zhao-Shea R, McIntosh JM, Gardner PD, Tapper AR (2012) Nicotine persistently activates ventral tegmental area dopaminergic neurons via nicotinic acetylcholine receptors containing alpha4 and alpha6 subunits. Mol Pharmacol 81:541-548.
40. London ED, Connolly RJ, Szikszay M, Wamsley JK, Dam M (1988) Effects of nicotine on local cerebral glucose utilization in the rat. J Neurosci 8:3920-3928.
41. Markou A, Paterson NE (2001) The nicotinic antagonist methyllycaconitine has differential effects on nicotine self-administration and nicotine withdrawal in the rat. Nicotine Tob Res 3:361-373.
42. McLaughlin J, See RE (2003) Selective inactivation of the dorsomedial prefrontal cortex and the basolateral amygdala attenuates conditioned-cued reinstatement of extinguished cocaine-seeking behavior in rats. Psychopharmacology (Berl) 168:57-65.
43. Mendelson JH, Goletiani N, Sholar MB, Siegel AJ, Mello NK (2008) Effects of smoking successive low- and high-nicotine cigarettes on hypothalamic-pituitary-adrenal axis hormones and mood in men. Neuropsychopharmacology 33:749-760.
44. Meyer EM, Tay ET, Papke RL, Meyers C, Huang GL, de Fiebre CM (1997) 3-[2,4-Dimethoxybenzylidene]anabaseine (DMXB) selectively activates rat alpha7 receptors and improves memory- related behaviors in a mecamylamine-sensitive manner. Brain Res 768:49-56.
45. Mineur YS, Picciotto MR (2010) Nicotine receptors and depression: revisiting and revising the cholinergic hypothesis. Trends Pharmacol Sci 31:580-586.
46. Mugnaini M, Garzotti M, Sartori I, Pilla M, Repeto P, Heidbreder CA, Tessari M (2006) Selective down-regulation of [(125)I] Y0-alpha-conotoxin MII binding in rat mesostriatal dopamine pathway following continuous infusion of nicotine. Neuroscience 137:565-572.
47. Naqvi NH, Bechara A (2009) The hidden island of addiction: the insula. Trends Neurosci 32:56-67.
48. Naqvi NH, Rudrauf D, Damasio H, Bechara A (2007) Damage to the insula disrupts addiction to cigarette smoking. Science 315:531-534.
49. Nyback H, Nordberg A, Langstrom B, Halldin C, Hartvig P, Ahlin A, Swahn CG, Sedvall G (1989) Attempts to visualize nicotinic receptors in the brain of monkey and man by positron emission tomography. Prog Brain Res 79:313-319.
50. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. San Diego, CA: Academic Press.
51. Phelps EA, LeDoux JE (2005) Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48:175-187.
52. Picciotto MR, Kenny PJ (2013) Molecular mechanisms underlying behaviors related to nicotine addiction. Cold Spring Harb Perspect Med 3:a012112.
53. Ray JP, Price JL (1993) The organization of projections from the mediodorsal nucleus of the thalamus to orbital and medial prefrontal cortex in macaque monkeys. J Comp Neurol 337:1-31.
54. Rezvani AH, Levin ED (2001) Cognitive effects of nicotine. Biol Psychiatry 49:258-267.
55. Risinger FO, Oakes RA (1995) Nicotine-induced conditioned place preference and conditioned place aversion in mice. Pharmacol Biochem Behav 51:457-461.
56. Salminen O, Lahtinen S, Ahtee L (1996) Expression of Fos protein in various rat brain areas following acute nicotine and diazepam. Pharmacol Biochem Behav 54:241-248.
57. See RE, Fuchs RA, Ledford CC, McLaughlin J (2003) Drug addiction, relapse, and the amygdala. Ann NY Acad Sci 985:294-307.
58. Sheline YI, Barch DM, Donnelly JM, Ollinger JM, Snyder AZ, Mintun MA (2001) Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study. Biol Psychiatry 50:651-658.
59. Shmuel A, Augath M, Oeltermann A, Logothetis NK (2006) Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1. Nat Neurosci 9:569-577.
60. Shram MJ, Funk D, Li Z, Le AD (2007) Acute nicotine enhances c-fos mRNA expression differentially in reward-related substrates of adolescent and adult rat brain. Neurosci Lett 418:286-291.
61. Siegle GJ, Steinhauer SR, Thase ME, Stenger VA, Carter CS (2002) Cant shake that feeling: event-related fMRI assessment of sustained amygdala activity in response to emotional information in depressed individuals. Biol Psychiatry 51:693-707.
62. Sihver W, Gillberg PG, Nordberg A (1998) Laminar distribution of nicotinic receptor subtypes in human cerebral cortex as determined by [3H](-)nicotine, [3H]cytisine and [3H]epibatidine in vitro autoradiography. Neuroscience 85:1121-1133.
63. Spina L, Fenu S, Longoni R, Rivas E, Di CG (2006) Nicotine-conditioned single-trial place preference: selective role of nucleus accumbens shell dopamine D1 receptors in acquisition. Psychopharmacology (Berl) 184:447-455.
64. Stein EA, Pankiewicz J, Harsch HH, Cho JK, Fuller SA, Hoffmann RG, Hawkins M, Rao SM, Bandettini PA, Bloom AS (1998) Nicotine- induced limbic cortical activation in the human brain: a functional MRI study. Am J Psychiatry 155:1009-1015.
65. Steward CA, Marsden CA, Prior MJ, Morris PG, Shah YB (2005) Methodological considerations in rat brain BOLD contrast pharmacological MRI. Psychopharmacology (Berl) 180:687-704.
66. Swanson LW (1999) Brain Maps: structure of the rat brain. Boston, MA: Elsevier Science.
67. Tizabi Y, Copeland RL, Jr., Louis VA, Taylor RE (2002) Effects of combined systemic alcohol and central nicotine administration into ventral tegmental area on dopamine release in the nucleus accumbens. Alcohol Clin Exp Res 26:394-399.
68. Toll L, Zaveri NT, Polgar WE, Jiang F, Khroyan TV, Zhou W, Xie XS, Stauber GB, Costello MR, Leslie FM (2012) AT-1001: a high affinity and selective alpha3beta4 nicotinic acetylcholine receptor antagonist blocks nicotine self-administration in rats. Neuropsychopharmacology 37:1367-1376.
69. Tomasi D, Volkow ND (2013) Striatocortical pathway dysfunction in addiction and obesity: differences and similarities. Crit Rev Biochem Mol Biol 48:1-19.
70. Tsurugizawa T, Uematsu A, Uneyama H, Torii K (2010) Effects of isoflurane and alpha-chloralose anesthesia on BOLD fMRI responses to ingested L-glutamate in rats. Neuroscience 165:244-251.
71. Tucha O, Lange KW (2004) Effects of nicotine chewing gum on a real-life motor task: a kinematic analysis of handwriting movements in smokers and non-smokers. Psychopharmacology (Berl) 173:49-56.
72. Tye KM, Stuber GD, de RB, Bonci A, Janak PH (2008) Rapid strengthening of thalamo-amygdala synapses mediates cuereward learning. Nature 453:1253-1257.
73. Vlachou S, Markou A (2011) Intracranial Self-Stimulation. In: Animal Models of Drug Addiction (Mary C. Olmstead, ed), pp 3-56. New York: Humana Press.
74. Volkow ND, Fowler JS (2000) Addiction, a disease of compulsion and drive: involvement of the orbitofrontal cortex. Cereb Cortex 10:318-325.
75. Volkow ND, Fowler JS, Wang GJ, Hitzemann R, Logan J, Schlyer DJ, Dewey SL, Wolf AP (1993) Decreased dopamine D2 receptor availability is associated with reduced frontal metabolism in cocaine abusers. Synapse 14:169-177.
76. Volkow ND, Wang GJ, Fowler JS, Logan J, Gatley SJ, Hitzemann R, Chen AD, Dewey SL, Pappas N (1997) Decreased striatal dopaminergic responsiveness in detoxified cocaine-dependent subjects. Nature 386:830-833.
77. Volkow ND, Wang GJ, Fowler JS, Logan J, Hitzemann R, Ding YS, Pappas N, Shea C, Piscani K (1996) Decreases in dopamine receptors but not in dopamine transporters in alcoholics. Alcohol Clin Exp Res 20:1594-1598.
78. Walters CL, Brown S, Changeux JP, Martin B, Damaj MI (2006) The beta2 but not alpha7 subunit of the nicotinic acetylcholine receptor is required for nicotine-conditioned place preference in mice. Psychopharmacology (Berl) 184: 339-344.
79. Watkins SS, Epping-Jordan MP, Koob GF, Markou A (1999) Blockade of nicotine self-administration with nicotinic antagonists in rats. Pharmacol Biochem Behav 62:743-751.
80. West RJ, Jarvis MJ (1986) Effects of nicotine on finger tapping rate in non-smokers. Pharmacol Biochem Behav 25:727-731.
81. Zuo Y, Lu H, Vaupel DB, Zhang Y, Chefer SI, Rea WR, Moore AV, Yang Y, Stein EA (2011) Acute nicotine-induced tachyphylaxis is differentially manifest in the limbic system. Neuropsychopharmacology 36:2498-2512.