Divergent functional effects of sazetidine-A and varenicline during nicotine withdrawal

Neuropsychopharmacology

Volumn 38, Issue 10, 2013, Pages 2035-2047

  Turner, Jill R ^a   Wilkinson, Derek S ^b   Poole, Rachel Lf ^b   Gould, Thomas J ^b   Carlson, Gregory C ^a   Blendy, Julie A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b TEMPLE UNIVERSITY   (United States)

Author keywords

anxiety; hippocampus; neuronal nicotinic acetylcholine receptor (nAChR); nicotine withdrawal; novelty induced hypophagia (NIH) test; voltage sensitive dye imaging (VSDi)

Indexed keywords

NICOTINE; NICOTINIC AGENT; SAZETIDINE A; UNCLASSIFIED DRUG; VARENICLINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; CONTROLLED STUDY; DRUG EXPOSURE; FUNCTIONAL DISSOCIATION; HYPOPHAGIA; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SMOKING CESSATION; VOLTAGE SENSITIVE DYE IMAGING; WITHDRAWAL SYNDROME;

ANIMALS; ANXIETY; AZETIDINES; BENZAZEPINES; CEREBRAL CORTEX; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG PARTIAL AGONISM; EVOKED POTENTIALS; HIPPOCAMPUS; MALE; MICE; MICROINJECTIONS; MOTOR ACTIVITY; NICOTINE; NICOTINIC AGONISTS; PYRIDINES; QUINOXALINES; RECEPTORS, NICOTINIC; SMOKING CESSATION; SUBSTANCE WITHDRAWAL SYNDROME; UP-REGULATION;

EID: 84882452010     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2013.105     Document Type: Article

References (104)

1. Anderson SM, Brunzell DH (2012). Low dose nicotine and antagonism of beta2 subunit containing nicotinic acetylcholine receptors have similar effects on affective behavior in mice. PLoS One 7: e48665.
2. Ang CW, Carlson GC, Coulter DA (2005). Hippocampal CA1 circuitry dynamically gates direct cortical inputs preferentially at theta frequencies. J Neurosci 25: 9567-9580.
3. Avalos M, Parker MJ, Maddox FN, Carroll FI, Luetje CW (2002). Effects of pyridine ring substitutions on affinity, efficacy, and subtype selectivity of neuronal nicotinic receptor agonist epibatidine. J Pharmacol Exp Ther 302: 1246-1252.
4. Azizian A, Monterosso J, O'Neill J, London ED (2009). Magnetic resonance imaging studies of cigarette smoking. Handb Exp Pharmacol 113-143.
5. Balu DT, Turner JR, Brookshire BR, Hill-Smith TE, Blendy JA, Lucki I (2013). Brain monoamines and antidepressant-like responses in MRL/MpJ versus C57BL/6J mice. Neuropharmacology 67: 503-510.
6. Bannerman DM, Deacon RM, Offen S, Friswell J, Grubb M, Rawlins JN (2002). Double dissociation of function within the hippocampus: spatial memory and hyponeophagia. Behav Neurosci 116: 884-901.
7. Bannerman DM, Grubb M, Deacon RM, Yee BK, Feldon J, Rawlins JN (2003). Ventral hippocampal lesions affect anxiety but not spatial learning. Behav Brain Res 139: 197-213.
8. Bannerman DM, Rawlins JN, McHugh SB, Deacon RM, Yee BK, Bast T et al (2004). Regional dissociations within the hippocampus- memory and anxiety. Neurosci Biobehav Rev 28: 273-283.
9. Bechtholt AJ, Hill TE, Lucki I (2007a). Anxiolytic effect of serotonin depletion in the novelty-induced hypophagia test. Psychopharmacology (Berl) 190: 531-540.
10. Bechtholt AJ, Valentino RJ, Lucki I (2007b). Overlapping and distinct brain regions associated with the anxiolytic effects of chlordiazepoxide and chronic fluoxetine. Neuropsychopharmacology 33: 2117-2130.
11. Bell KA, Shim H, Chen CK, McQuiston AR (2011). Nicotinic excitatory postsynaptic potentials in hippocampal CA1 interneurons are predominantly mediated by nicotinic receptors that contain alpha4 and beta2 subunits. Neuropharmacology 61: 1379-1388.
12. Benowitz NL (2009). Pharmacology of nicotine: addiction, smoking- induced disease, and therapeutics. Annu Rev Pharmacol Toxicol 49: 57-71.
13. Bremner JD, Randall P, Scott TM, Bronen RA, Seibyl JP, Southwick SM et al (1995). MRI-based measurement of hippocampal volume in patients with combat-related posttraumatic stress disorder. Am J Psychiatry 152: 973-981.
14. Brody AL, Mandelkern MA, London ED, Olmstead RE, Farahi J, Scheibal D et al (2006). Cigarette smoking saturates brain alpha 4 beta 2 nicotinic acetylcholine receptors. Arch Gen Psychiatry 63: 907-915.
15. Caldarone BJ, Wang D, Paterson NE, Manzano M, Fedolak A, Cavino K et al (2011). Dissociation between duration of action in the forced swim test in mice and nicotinic acetylcholine receptor occupancy with sazetidine, varenicline, and 5-I-A85380. Psychopharmacology (Berl) 217: 199-210.
16. CDC (2007). Cigarette smoking among adults-United States, 2006. Morbid Mortal Wkly Rep 56: 1157-1161.
17. Coe JW, Brooks PR, Vetelino MG, Wirtz MC, Arnold EP, Huang J et al (2005). Varenicline: an alpha4beta2 nicotinic receptor partial agonist for smoking cessation. J Med Chem 48: 3474-3477.
18. Cole J, Toga AW, Hojatkashani C, Thompson P, Costafreda SG, Cleare AJ et al (2010). Subregional hippocampal deformations in major depressive disorder. J Affect Disord 126: 272-277.
19. Corrigall WA, Coen KM, Adamson KL (1994). Self-administered nicotine activates the mesolimbic dopamine system through the ventral tegmental area. Brain Res 653: 278-284.
20. Corrigall WA, Franklin KB, Coen KM, Clarke PB (1992). The mesolimbic dopaminergic system is implicated in the reinforcing effects of nicotine. Psychopharmacology (Berl) 107: 285-289.
21. Cosgrove KP, Batis J, Bois F, Maciejewski PK, Esterlis I, Kloczynski T et al (2009). beta2-Nicotinic acetylcholine receptor availability during acute and prolonged abstinence from tobacco smoking. Arch Gen Psychiatry 66: 666-676.
22. Costall B, Kelly ME, Naylor RJ, Onaivi ES (1989). The actions of nicotine and cocaine in a mouse model of anxiety. Pharmacol Biochem Behav 33: 197-203.
23. Dalla C, Whetstone AS, Hodes GE, Shors TJ (2009). Stressful experience has opposite effects on dendritic spines in the hippocampus of cycling versus masculinized females. Neurosci Lett 449: 52-56.
24. Dani JA, Harris RA (2005). Nicotine addiction and comorbidity with alcohol abuse and mental illness. Nat Neurosci 8: 1465-1470.
25. Davis JA, Gould TJ (2009). Hippocampal nAChRs mediate nicotine withdrawal-related learning deficits. Eur Neuropsychopharmacol 19: 551-561.
26. Davis JA, Kenney JW, Gould TJ (2007). Hippocampal alpha4beta2 nicotinic acetylcholine receptor involvement in the enhancing effect of acute nicotine on contextual fear conditioning. J Neurosci 27: 10870-10877.
27. Degroot A, Treit D (2003). Septal GABAergic and hippocampal cholinergic systems interact in the modulation of anxiety. Neuroscience 117: 493-501.
28. Degroot A, Treit D (2004). Anxiety is functionally segregated within the septo-hippocampal system. Brain Res 1001: 60-71.
29. Deuther-Conrad W, Wevers A, Becker G, Schildan A, Patt M, Sabri O et al (2006). Autoradiography of 2-[18F]F-A-85380 on nicotinic acetylcholine receptors in the porcine brain in vitro. Synapse (New York, NY) 59: 201-210.
30. DiMatteo MR, Lepper HS, Croghan TW (2000). Depression is a risk factor for noncompliance with medical treatment: meta-analysis of the effects of anxiety and depression on patient adherence. Arch Intern Med 160: 2101-2107.
31. Dulawa SC, Hen R (2005). Recent advances in animal models of chronic antidepressant effects: the novelty-induced hypophagia test. Neurosci Biobehav Rev 29: 771-783.
32. Froeliger B, Kozink RV, Rose JE, Behm FM, Salley AN, McClernon FJ (2010). Hippocampal and striatal gray matter volume are associated with a smoking cessation treatment outcome: results of an exploratory voxel-based morphometric analysis. Psychopharmacology (Berl) 210: 577-583.
33. Gamble-George JC, Conger JR, Hartley ND, Gupta P, Sumislawski JJ, Patel S (2013). Dissociable effects of CB1 receptor blockade on anxiety-like and consummatory behaviors in the noveltyinduced hypophagia test in mice. Psychopharmacology (Berl).
34. Gatt JM, Nemeroff CB, Dobson-Stone C, Paul RH, Bryant RA, Schofield PR et al (2009). Interactions between BDNF Val66Met polymorphism and early life stress predict brain and arousal pathways to syndromal depression and anxiety. Mol Psychiatry 14: 681-695.
35. Goeldner C, Spooren W, Wichmann J, Prinssen EP (2012). Further characterization of the prototypical nociceptin/orphanin FQ peptide receptor agonist Ro 64-6198 in rodent models of conflict anxiety and despair. Psychopharmacology (Berl) 222: 203-214.
36. Gonzales D, Rennard SI, Nides M, Oncken C, Azoulay S, Billing CB et al (2006). Varenicline, an alpha4beta2 nicotinic acetylcholine receptor partial agonist, vs sustained-release bupropion and placebo for smoking cessation: a randomized controlled trial. JAMA 296: 47-55.
37. Gray JA, McNaughton N (1996). The neuropsychology of anxiety: reprise. Nebr Symp Motiv 43: 61-134.
38. Gray JA, McNaughton N (2000). The Neuropsychology of Anxiety: An Enquiry into the Functions of the Septo-Hippocampal System. 2nd edn Oxford University Press: Oxford, New York, xvi, 424 p..
39. Grieder TE, George O, Tan H, George SR, Le Foll B, Laviolette SR et al (2012). Phasic D1 and tonic D2 dopamine receptor signaling double dissociate the motivational effects of acute nicotine and chronic nicotine withdrawal. Proc Natl Acad Sci USA 109: 3101-3106.
40. Gur TL, Conti AC, Holden J, Bechtholt AJ, Hill TE, Lucki I et al (2007). cAMP response element-binding protein deficiency allows for increased neurogenesis and a rapid onset of antidepressant response. J Neurosci 27: 7860-7868.
41. Hahn T, Dresler T, Plichta MM, Ehlis AC, Ernst LH, Markulin F et al (2010). Functional amygdala-hippocampus connectivity during anticipation of aversive events is associated with Gray's trait "sensitivity to punishment". Biol Psychiatry 68: 459-464.
42. Hendrickson LM, Zhao-Shea R, Pang X, Gardner PD, Tapper AR (2010). Activation of alpha4*nAChRs is necessary and sufficient for varenicline-induced reduction of alcohol consumption. J Neurosci 30: 10169-10176.
43. Hogle JM, Kaye JT, Curtin JJ (2010). Nicotine withdrawal increases threat-induced anxiety but not fear: neuroadaptation in human addiction. Biol Psychiatry 68: 719-725.
44. Houghtling RA, Davila-Garcia MI, Kellar KJ (1995). Characterization of (/)()[3H]epibatidine binding to nicotinic cholinergic receptors in rat and human brain. Mol Pharmacol 48: 280-287.
45. Hussmann GP, Turner JR, Lomazzo E, Venkatesh R, Cousins V, Xiao Y et al (2012). Chronic sazetidine-A at behaviorally active doses does not increase nicotinic cholinergic receptors in rodent brain. J Pharmacol Exp Ther 343: 441-450.
46. Irvine EE, Cheeta S, File SE (2001). Tolerance to nicotine's effects in the elevated plus-maze and increased anxiety during withdrawal. Pharmacol Biochem Behav 68: 319-325.
47. Jackson KJ, Martin BR, Changeux JP, Damaj MI (2008). Differential role of nicotinic acetylcholine receptor subunits in physical and affective nicotine withdrawal signs. J Pharmacol Exp Ther 325: 302-312.
48. Jackson KJ, McIntosh JM, Brunzell DH, Sanjakdar SS, Damaj MI (2009). The role of alpha6-containing nicotinic acetylcholine receptors in nicotine reward and withdrawal. J Pharmacol Exp Ther 331: 547-554.
49. Joels M, Karst H, Alfarez D, Heine VM, Qin Y, van Riel E et al (2004). Effects of chronic stress on structure and cell function in rat hippocampus and hypothalamus. Stress 7: 221-231.
50. Joels M, Krugers H, Karst H (2008). Stress-induced changes in hippocampal function. Prog Brain Res 167: 3-15.
51. Jonkman S, Henry B, Semenova S, Markou A (2005). Mild anxiogenic effects of nicotine withdrawal in mice. Eur J Pharmacol 516: 40-45.
52. Kalisch R, Schubert M, Jacob W, Kessler MS, Hemauer R, Wigger A et al (2006). Anxiety and hippocampus volume in the rat. Neuropsychopharmacology 31: 925-932.
53. Kenney JW, Adoff MD, Wilkinson DS, Gould TJ (2011). The effects of acute, chronic, and withdrawal from chronic nicotine on novel and spatial object recognition in male C57BL/6J mice. Psychopharmacology (Berl) 217: 353-365.
54. Kenney JW, Gould TJ (2008). Modulation of hippocampusdependent learning and synaptic plasticity by nicotine. Mol Neurobiol 38: 101-121.
55. Kenney JW, Raybuck JD, Gould TJ (2012). Nicotinic receptors in the dorsal and ventral hippocampus differentially modulate contextual fear conditioning. Hippocampus 22: 1681-1690.
56. Kozikowski AP, Eaton JB, Bajjuri KM, Chellappan SK, Chen Y, Karadi S et al (2009). Chemistry and pharmacology of nicotinic ligands based on 6-[5-(azetidin-2-ylmethoxy)pyridin-3-yl]hex- 5-yn-1-ol (AMOP-H-OH) for possible use in depression. ChemMedChem 4: 1279-1291.
57. Laviolette SR, Lauzon NM, Bishop SF, Sun N, Tan H (2008). Dopamine signaling through D1-like versus D2-like receptors in the nucleus accumbens core versus shell differentially modulates nicotine reward sensitivity. J Neurosci 28: 8025-8033.
58. Laviolette SR, van der Kooy D (2003). Blockade of mesolimbic dopamine transmission dramatically increases sensitivity to the rewarding effects of nicotine in the ventral tegmental area. Mol Psychiatry 8: 50-59 9.
59. Lee JH, Jones PG, Bybee K, O'Keefe JH (2008). A longer course of varenicline therapy improves smoking cessation rates. Prev Cardiol 11: 210-214.
60. Levin ED, McClernon FJ, Rezvani AH (2006). Nicotinic effects on cognitive function: behavioral characterization, pharmacological specification, and anatomic localization. Psychopharmacology (Berl) 184: 523-539.
61. Levin ED, Rezvani AH, Xiao Y, Slade S, Cauley M, Wells C et al (2010). Sazetidine-A, a selective alpha4beta2 nicotinic receptor desensitizing agent and partial agonist, reduces nicotine self-administration in rats. J Pharmacol Exp Ther 332: 933-939.
62. Lewis MC, Gould TJ (2007). Reversible inactivation of the entorhinal cortex disrupts the establishment and expression of latent inhibition of cued fear conditioning in C57BL/6 mice. Hippocampus 17: 462-470.
63. Marks MJ, Burch JB, Collins AC (1983). Effects of chronic nicotine infusion on tolerance development and nicotinic receptors. J Pharmacol Exp Ther 226: 817-825.
64. Marrosu F, Portas C, Mascia MS, Casu MA, Fa M, Giagheddu M et al (1995). Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep-wake cycle in freely moving cats. Brain Res 671: 329-332.
65. McClernon FJ, Gilbert DG (2004). Human functional neuroimaging in nicotine and tobacco research: basics, background, and beyond. Nicotine Tob Res 6: 941-959.
66. McClernon FJ, Kozink RV, Rose JE (2008). Individual differences in nicotine dependence, withdrawal symptoms, and sex predict transient fMRI-BOLD responses to smoking cues. Neuropsychopharmacology 33: 2148-2157.
67. McEwen BS (2001). Plasticity of the hippocampus: adaptation to chronic stress and allostatic load. Ann NY Acad Sci 933: 265-277.
68. McEwen BS, Magarinos AM (2001). Stress and hippocampal plasticity: implications for the pathophysiology of affective disorders. Hum Psychopharmacol 16(S1): S7-S19.
69. McHugh SB, Deacon RM, Rawlins JN, Bannerman DM (2004). Amygdala and ventral hippocampus contribute differentially to mechanisms of fear and anxiety. Behav Neurosci 118: 63-78.
70. McHugh SB, Fillenz M, Lowry JP, Rawlins JN, Bannerman DM (2011). Brain tissue oxygen amperometry in behaving rats demonstrates functional dissociation of dorsal and ventral hippocampus during spatial processing and anxiety. Eur J Neurosci 33: 322-337.
71. McQuiston AR (2010). Cholinergic modulation of excitatory synaptic input integration in hippocampal CA1. J Physiol 588(Pt 19): 3727-3742.
72. Merali Z, Levac C, Anisman H (2003). Validation of a simple, ethologically relevant paradigm for assessing anxiety in mice. Biol Psychiatry 54: 552-565.
73. Mineur YS, Einstein EB, Seymour PA, Coe JW, O'Neill BT, Rollema H et al (2011). alpha4beta2 nicotinic acetylcholine receptor partial agonists with low intrinsic efficacy have antidepressantlike properties. Behav Pharmacol 22: 291-299.
74. Nicolas L, Kolb Y, Prinssen E (2006). A combined marble buryinglocomotor activity test in mice: a practical screening test with sensitivity to different classes of anxiolytics and antidepressants. Eur J Pharmacol 547: 106-115.
75. O'Connor EC, Parker D, Rollema H, Mead AN (2010). The alpha4beta2 nicotinic acetylcholine-receptor partial agonist varenicline inhibits both nicotine self-administration following repeated dosing and reinstatement of nicotine seeking in rats. Psychopharmacology (Berl) 208: 365-376.
76. Onksen JL, Briand LA, Galante RJ, Pack AI, Blendy JA (2012). Running-induced anxiety is dependent on increases in hippocampal neurogenesis. Genes Brain Behav 11: 529-538.
77. Ortinski PI, Dong J, Mungenast A, Yue C, Takano H, Watson DJ et al (2010). Selective induction of astrocytic gliosis generates deficits in neuronal inhibition. Nat Neurosci 13: 584-591.
78. Paxinos G, Franklin KBJ (2001). The Mouse Brain in Stereotaxic Coordinates, 2nd edn. Academic Press: San Diego, CA. Penton RE, Quick MW, Lester RA (2011). Short- and long-lasting consequences of in vivo nicotine treatment on hippocampal excitability. J Neurosci 31: 2584-2594.
79. Picciotto MR, Addy NA, Mineur YS, Brunzell DH (2008). It is not "either/or": Activation and desensitization of nicotinic acetylcholine receptors both contribute to behaviors related to nicotine addiction and mood. Prog Neurobiol 84: 329-342.
80. Picciotto MR, Brunzell DH, Caldarone BJ (2002). Effect of nicotine and nicotinic receptors on anxiety and depression. Neuroreport 13: 1097-1106.
81. Piper ME, Cook JW, Schlam TR, Jorenby DE, Baker TB (2011). Anxiety diagnoses in smokers seeking cessation treatment: relations with tobacco dependence, withdrawal, outcome and response to treatment. Addiction 106: 418-427.
82. Polosa R, Benowitz NL (2011). Treatment of nicotine addiction: present therapeutic options and pipeline developments. Trends Pharmacol Sci 32: 281-289.
83. Pomerleau OF, Pomerleau CS, Mehringer AM, Snedecor SM, Ninowski R, Sen A (2005). Nicotine dependence, depression, and gender: characterizing phenotypes based on withdrawal discomfort, response to smoking, and ability to abstain. Nicotine Tob Res 7: 91-102.
84. Raybuck J, Portugal G, Lerman C, Gould T (2008). Varenicline ameliorates nicotine withdrawal-induced learning deficits in C57BL/6 mice. Behav Neurosci 122: 1166-1171.
85. Rezvani AH, Cauley M, Sexton H, Xiao Y, Brown ML, Paige MA et al (2011). Sazetidine-A, a selective alpha4beta2 nicotinic acetylcholine receptor ligand: effects on dizocilpine and scopolamine-induced attentional impairments in female Sprague- Dawley rats. Psychopharmacology (Berl) 215: 621-630.
86. Rezvani AH, Levin ED (2001). Cognitive effects of nicotine. Biol Psychiatry 49: 258-267.
87. Rezvani AH, Slade S, Wells C, Petro A, Lumeng L, Li TK et al (2010). Effects of sazetidine-A, a selective alpha4beta2 nicotinic acetylcholine receptor desensitizing agent on alcohol and nicotine self-administration in selectively bred alcohol-preferring (P) rats. Psychopharmacology (Berl) 211: 161-174.
88. Rollema H, Chambers LK, Coe JW, Glowa J, Hurst RS, Lebel LA et al (2007). Pharmacological profile of the alpha4beta2 nicotinic acetylcholine receptor partial agonist varenicline, an effective smoking cessation aid. Neuropharmacology 52: 985-994.
89. Rollema H, Guanowsky V, Mineur YS, Shrikhande A, Coe JW, Seymour PA et al (2009). Varenicline has antidepressant-like activity in the forced swim test and augments sertraline's effect. Eur J Pharmacol 605: 114-116.
90. Rollema H, Shrikhande A, Ward KM, Tingley FD 3rd, Coe JW, O'Neill BT et al (2010). Pre-clinical properties of the alpha4beta2 nicotinic acetylcholine receptor partial agonists varenicline, cytisine and dianicline translate to clinical efficacy for nicotine dependence. Br J Pharmacol 160: 334-345.
91. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S et al (2003). Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science (New York, NY) 301: 805-809.
92. Schwartz R, Kellar K (1983). Nicotinic cholinergic receptor binding sites in the brain: regulation in vivo. Science (New York, NY) 220: 214-216.
93. Shors TJ, Chua C, Falduto J (2001). Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. J Neurosci 21: 6292-6297.
94. Shors TJ, Gallegos RA, Breindl A (1997). Transient and persistent consequences of acute stress on long-term potentiation (LTP), synaptic efficacy, theta rhythms and bursts in area CA1 of the hippocampus. Synapse (New York, NY) 26: 209-217.
95. Stein MB, Koverola C, Hanna C, Torchia MG, McClarty B (1997). Hippocampal volume in women victimized by childhood sexual abuse. Psychol Med 27: 951-959.
96. Stoker AK, Semenova S, Markou A (2008). Affective and somatic aspects of spontaneous and precipitated nicotine withdrawal in C57BL/6J and BALB/cByJ mice. Neuropharmacology 54: 1223-1232.
97. Tonstad S, Tonnesen P, Hajek P, Williams KE, Billing CB, Reeves KR (2006). Effect of maintenance therapy with varenicline on smoking cessation: a randomized controlled trial. JAMA 296: 64-71.
98. Turner JR, Castellano LM, Blendy JA (2010). Nicotinic partial agonists varenicline and sazetidine-A have differential effects on affective behavior. J Pharmacol Exp Ther 334: 665-672.
99. Turner JR, Castellano LM, Blendy JA (2011). Parallel anxiolytic-like effects and upregulation of neuronal nicotinic acetylcholine receptors following chronic nicotine and varenicline. Nicotine Tob Res 13: 41-46.
100. Vaupel DB, Tella SR, Huso DL, Wagner VO 3rd, Mukhin AG, Chefer SI et al (2005). Pharmacological and toxicological evaluation of 2-fluoro-3-(2(S)- Azetidinylmethoxy)pyridine (2-FA- 85380), a ligand for imaging cerebral nicotinic acetylcholine receptors with positron emission tomography. J Pharmacol Exp Ther 312: 355-365.
101. Wilkinson DS, Turner JR, Blendy JA, Gould TJ (2013). Genetic background influences the effects of withdrawal from chronic nicotine on learning and high-Affinity nicotinic acetylcholine receptor binding in the dorsal and ventral hippocampus. Psychopharmacology (Berl) 225: 201-208.
102. Xiao Y, Fan H, Musachio JL, Wei ZL, Chellappan SK, Kozikowski AP et al (2006). Sazetidine-A, a novel ligand that desensitizes alpha4beta2 nicotinic acetylcholine receptors without activating them. Mol Pharmacol 70: 1454-1460.
103. Xiao Y, Kellar KJ (2004). The comparative pharmacology and up-regulation of rat neuronal nicotinic receptor subtype binding sites stably expressed in transfected mammalian cells. J Pharmacol Exp Ther 310: 98-107.
104. Zwart R, Carbone A, Moroni M, Bermudez E, Mogg A, Folly E et al (2008). Sazetidine-A is a potent and selective agonist at native and recombinant alpha4beta2 nicotinic acetylcholine receptors. Mol Pharmacol 73: 1838-1843..