Progesterone improves cognitive performance and attenuates smoking urges in abstinent smokers

Psychoneuroendocrinology

Volumn 36, Issue 1, 2011, Pages 123-132

  Sofuoglu, Mehmet ^a   Mouratidis, Maria ^b   Mooney, Marc ^c  

^a YALE UNIVERSITY   (United States)

^b NOTRE DAME OF MARYLAND UNIVERSITY   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Cognitive performance; Menstrual cycle phase; Nicotine dependence; Progesterone; Sex differences

Indexed keywords

CARBON MONOXIDE; ESTRADIOL; PLACEBO; PROGESTERONE;

ADULT; ARTICLE; BREATH ANALYSIS; CIGARETTE SMOKING; CLINICAL TRIAL; COGNITION; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DIGIT SYMBOL SUBSTITUTION TEST; DOSE RESPONSE; DOUBLE BLIND PROCEDURE; DRUG ABSORPTION; DRUG BLOOD LEVEL; DRUG DOSE COMPARISON; DRUG EFFICACY; ESTRADIOL BLOOD LEVEL; EVENING DOSAGE; FEMALE; FOLLICULAR PHASE; HUMAN; MAJOR CLINICAL STUDY; MALE; MORNING DOSAGE; NEUROPSYCHOLOGICAL TEST; OUTCOME ASSESSMENT; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; SELF REPORT; SMOKING CESSATION; STROOP INTERFERENCE TEST; TOBACCO DEPENDENCE;

ADOLESCENT; ADULT; COGNITION; DOUBLE-BLIND METHOD; ESTRADIOL; FEMALE; HUMANS; MALE; MIDDLE AGED; PLACEBOS; PROGESTERONE; SMOKING; SMOKING CESSATION; SUBSTANCE WITHDRAWAL SYNDROME; TASK PERFORMANCE AND ANALYSIS; YOUNG ADULT;

EID: 78649894217     PISSN: 03064530     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2010.07.005     Document Type: Article

References (92)

1. Allen S.S., Bade T., Center B., Finstad D., Hatsukami D. Menstrual phase effects on smoking relapse. Addiction 2008, 103:809-821.
2. American Psychiatric Association. Diagnostic and statistical manual of mental disorders: DSM-IV. 4th ed. Washington, DC: American Psychiatric Association; 1994.
3. Anker J.J., Holtz N.A., Zlebnik N., Carroll M.E. Effects of allopregnanolone on the reinstatement of cocaine-seeking behavior in male and female rats. Psychopharmacology (Berl) 2009, 203:63-72.
4. Anker J.J., Larson E.B., Gliddon L.A., Carroll M.E. Effects of progesterone on the reinstatement of cocaine-seeking behavior in female rats. Exp. Clin. Psychopharmacol. 2007, 15:472-480.
5. Becker J.B. Gender differences in dopaminergic function in striatum and nucleus accumbens. Pharmacol. Biochem. Behav. 1999, 64:803-812.
6. Becker J.B., Hu M. Sex differences in drug abuse. Front. Neuroendocrinol. 2008, 29:36-47.
7. Bell S.L., Taylor R.C., Singleton E.G., Henningfield J.E., Heishman S.J. Smoking after nicotine deprivation enhances cognitive performance and decreases tobacco craving in drug abusers [in process citation]. Nicotine Tob. Res. 1999, 1:45-52.
8. Benowitz N.L., Gourlay S.G. Cardiovascular toxicity of nicotine: implications for nicotine replacement therapy. J. Am. Coll. Cardiol. 1997, 29:1422-1431.
9. Benowitz N.L., Jacob P.I., Ahijevich K., Jarvis M.J., Hall S., LeHouzec J., et al. Biochemical verification of tobacco use and cessation. Report from the srnt subcommittee on biochemical verification. Nicotine Tob. Res. 2002, 4:149-159.
10. Bisaga A., Padilla M., Garawi F., Sullivan M.A., Haney M. Effects of alternative reinforcer and craving on the choice to smoke cigarettes in the laboratory. Hum. Psychopharmacol. 2007, 22:41-47.
11. Brandon T.H., Tiffany S.T., Obremski K.M., Baker T.B. Postcessation cigarette use: the process of relapse. Addict. Behav. 1990, 15:105-114.
12. Brinton R.D., Thompson R.F., Foy M.R., Baudry M., Wang J., Finch C.E., et al. Progesterone receptors: form and function in brain. Front. Neuroendocrinol. 2008, 29:313-339.
13. Bullock A.E., Clark A.L., Grady S.R., Robinson S.F., Slobe B.S., Marks M.J., et al. Neurosteroids modulate nicotinic receptor function in mouse striatal and thalamic synaptosomes. J. Neurochem. 1997, 68:2412-2423.
14. Callachan H., Cottrell G.A., Hather N.Y., Lambert J.J., Nooney J.M., Peters J.A. Modulation of the gabaa receptor by progesterone metabolites. Proc. R. Soc. Lond. B: Biol. Sci. 1987, 231:359-369.
15. Carpenter M.J., Upadhyaya H.P., LaRowe S.D., Saladin M.E., Brady K.T. Menstrual cycle phase effects on nicotine withdrawal and cigarette craving: a review. Nicotine Tob. Res. 2006, 8:627-638.
16. Cepeda-Benito A., Reynoso J.T., Erath S. Meta-analysis of the efficacy of nicotine replacement therapy for smoking cessation: differences between men and women. J. Consult. Clin. Psychol. 2004, 72:712-722.
17. Chabbert Buffet N., Djakoure C., Maitre S.C., Bouchard P. Regulation of the human menstrual cycle. Front. Neuroendocrinol. 1998, 19:151-186.
18. Chesnoy-Marchais D. Progesterone and allopregnanolone enhance the miniature synaptic release of glycine in the rat hypoglossal nucleus. Eur. J. Neurosci. 2009, 30:2100-2111.
19. Choi J.M., Romeo R.D., Brake W.G., Bethea C.L., Rosenwaks Z., McEwen B.S. Estradiol increases pre- and post-synaptic proteins in the ca1 region of the hippocampus in female rhesus macaques (macaca mulatta). Endocrinology 2003, 144:4734-4738.
20. Colman G.J., Joyce T. Trends in smoking before, during, and after pregnancy in ten states. Am. J. Prev. Med. 2003, 24:29-35.
21. Cox L.S., Tiffany S.T., Christen A.G. Evaluation of the brief questionnaire of smoking urges (qsu-brief) in laboratory and clinical settings. Nicotine Tob. Res. 2001, 3:7-16.
22. Cummings J.A., Brizendine L. Comparison of physical and emotional side effects of progesterone or medroxyprogesterone in early postmenopausal women. Menopause 2002, 9:253-263.
23. Dar D.E., Zinder O. Short term effect of steroids on catecholamine secretion from bovine adrenal medulla chromaffin cells. Neuropharmacology 1997, 36:1783-1788.
24. de Lignieres B. Oral micronized progesterone. Clin. Ther. 1999, 21:41-60. (discussion 41-42).
25. de Lignieres B., Silberstein S. Pharmacodynamics of oestrogens and progestogens. Cephalalgia 2000, 20:200-207.
26. Del Rio G., Velardo A., Menozzi R., Zizzo G., Tavernari V., Venneri M.G., et al. Acute estradiol and progesterone administration reduced cardiovascular and catecholamine responses to mental stress in menopausal women. Neuroendocrinology 1998, 67:269-274.
27. Eissenberg T., Griffiths R.R., Stitzer M.L. Mecamylamine does not precipitate withdrawal in cigarette smokers. Psychopharmacology (Berl) 1996, 127:328-336.
28. Evans S.M., Foltin R.W. Exogenous progesterone attenuates the subjective effects of smoked cocaine in women, but not in men. Neuropsychopharmacology 2006, 31:659-674.
29. Feltenstein M.W., Byrd E.A., Henderson A.R., See R.E. Attenuation of cocaine-seeking by progesterone treatment in female rats. Psychoneuroendocrinology 2009, 34:343-352.
30. Finn D.A., Beckley E.H., Kaufman K.R., Ford M.M. Manipulation of gabaergic steroids: sex differences in the effects on alcohol drinking- and withdrawal-related behaviors. Horm. Behav. 2010, 57:12-22.
31. Ford M.M., Nickel J.D., Phillips T.J., Finn D.A. Neurosteroid modulators of gaba(a) receptors differentially modulate ethanol intake patterns in male c57bl/6j mice. Alcohol. Clin. Exp. Res. 2005, 29:1630-1640.
32. Frye C.A. Progestins influence motivation, reward, conditioning, stress, and/or response to drugs of abuse. Pharmacol. Biochem. Behav. 2007, 86:209-219.
33. Frye C.A., Walf A.A. Progesterone enhances performance of aged mice in cortical or hippocampal tasks. Neurosci. Lett. 2008, 437:116-120.
34. Frye C.A., Walf A.A. Progesterone to ovariectomized mice enhances cognitive performance in the spontaneous alternation, object recognition, but not placement, water maze, and contextual and cued conditioned fear tasks. Neurobiol. Learn. Mem. 2008, 90:171-177.
35. Girdler S.S., O'Briant C., Steege J., Grewen K., Light K.C. A comparison of the effect of estrogen with or without progesterone on mood and physical symptoms in postmenopausal women. J. Womens Health Gend. Based Med. 1999, 8:637-646.
36. Golden C. Stroop Color and Word Test: A Manual for Clinical and Experimental Uses 1978, Stoelting Company, Woodale.
37. Gron G., Friess E., Herpers M., Rupprecht R. Assessment of cognitive performance after progesterone administration in healthy male volunteers. Neuropsychobiology 1997, 35:147-151.
38. Harburger L.L., Pechenino A.S., Saadi A., Frick K.M. Post-training progesterone dose-dependently enhances object, but not spatial, memory consolidation. Behav Brain Res 2008, 194:174-180.
39. Heatherton T.F., Kozlowski L.T., Frecker R.C., Fagerstrom K.O. The fagerstrom test for nicotine dependence: a revision of the fagerstrom tolerance questionnaire. Br. J. Addict. 1991, 86:1119-1127.
40. Henderson V.W. Cognitive changes after menopause: influence of estrogen. Clin. Obstet. Gynecol. 2008, 51:618-626.
41. Hermsmeyer R.K., Thompson T.L., Pohost G.M., Kaski J.C. Cardiovascular effects of medroxyprogesterone acetate and progesterone: a case of mistaken identity?. Nat. Clin. Pract. Cardiovasc. Med. 2008, 5:387-395.
42. Herzog A.G. Catamenial epilepsy: definition, prevalence pathophysiology and treatment. Seizure 2008, 17:151-159.
43. Jodhka P.K., Kaur P., Underwood W., Lydon J.P., Singh M. The differences in neuroprotective efficacy of progesterone and medroxyprogesterone acetate correlate with their effects on bdnf expression. Endocrinology 2009.
44. Justice A.J., de Wit H. Acute effects of estradiol pretreatment on the response to d-amphetamine in women. Neuroendocrinology 2000, 71:51-59.
45. Kenford S.L., Fiore M.C., Jorenby D.E., Smith S.S., Wetter D., Baker T.B. Predicting smoking cessation. Who will quit with and without the nicotine patch. JAMA 1994, 271:589-594.
46. Kenford S.L., Smith S.S., Wetter D.W., Jorenby D.E., Fiore M.C., Baker T.B. Predicting relapse back to smoking: contrasting affective and physical models of dependence. J. Consult. Clin. Psychol. 2002, 70:216-227.
47. Lewis M.C., Orr P.T., Frick K.M. Differential effects of acute progesterone administration on spatial and object memory in middle-aged and aged female c57bl/6 mice. Horm. Behav. 2008, 54:455-462.
48. Majewska M.D. Steroid regulation of the gabaa receptor: ligand binding, chloride transport and behaviour. Ciba Found. Symp. 1990, 153:83-97.
49. Majewska M.D., Harrison N.L., Schwartz R.D., Barker J.L., Paul S.M. Steroid hormone metabolites are barbiturate-like modulators of the gaba receptor. Science 1986, 232:1004-1007.
50. Maki P.M. A systematic review of clinical trials of hormone therapy on cognitive function: effects of age at initiation and progestin use. Ann. N.Y. Acad. Sci. 2005, 1052:182-197.
51. Mancuso G., Warburton D.M., Melen M., Sherwood N., Tirelli E. Selective effects of nicotine on attentional processes. Psychopharmacology (Berl) 1999, 146:199-204.
52. McCoy S.J., Beal J.M., Watson G.H. Endocrine factors and postpartum depression. A selected review. J. Reprod. Med. 2003, 48:402-408.
53. McNair D., Lorr M., Dropperman L. Manual for Profile of Mood States 1971, Educational and Industrial Testing Services, San Diego, CA.
54. Morgan M.J., Davies G.M., Willner P. The questionnaire of smoking urges is sensitive to abstinence and exposure to smoking-related cues. Behav. Pharmacol. 1999, 10:619-626.
55. Nilsen J., Brinton R.D. Divergent impact of progesterone and medroxyprogesterone acetate (provera) on nuclear mitogen-activated protein kinase signaling. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:10506-10511.
56. Paradiso K., Sabey K., Evers A.S., Zorumski C.F., Covey D.F., Steinbach J.H. Steroid inhibition of rat neuronal nicotinic alpha4beta2 receptors expressed in hek 293 cells. Mol. Pharmacol. 2000, 58:341-351.
57. Patchev V.K., Hassan A.H., Holsboer D.F., Almeida O.F. The neurosteroid tetrahydroprogesterone attenuates the endocrine response to stress and exerts glucocorticoid-like effects on vasopressin gene transcription in the rat hypothalamus. Neuropsychopharmacology 1996, 15:533-540.
58. Pazol K., Northcutt K.V., Patisaul H.B., Wallen K., Wilson M.E. Progesterone and medroxyprogesterone acetate differentially regulate alpha4 subunit expression of gaba(a) receptors in the ca1 hippocampus of female rats. Physiol. Behav. 2009, 97:58-61.
59. PDR Physicians' Desk Reference: PDR 2009, Medical Economics Data, Montvale, NJ.
60. Pearson Murphy B.E., Allison C.M. Determination of progesterone and some of its neuroactive ring a-reduced metabolites in human serum. J. Steroid Biochem. Mol. Biol. 2000, 74:137-142.
61. Perkins K.A., Levine M., Marcus M., Shiffman S., D'Amico D., Miller A., et al. Tobacco withdrawal in women and menstrual cycle phase. J. Consult. Clin. Psychol. 2000, 68:176-180.
62. Petrie R.X., Deary I.J. Smoking and human information processing. Psychopharmacology 1989, 99:393-396.
63. Phillips S.M., Sherwin B.B. Variations in memory function and sex steroid hormones across the menstrual cycle. Psychoneuroendocrinology 1992, 17:497-506.
64. Provost S.C., Woodward R. Effects of nicotine gum on repeated administration of the stroop test. Psychopharmacology (Berl) 1991, 104:536-540.
65. Rapp S.R., Espeland M.A., Shumaker S.A., Henderson V.W., Brunner R.L., Manson J.E., et al. Effect of estrogen plus progestin on global cognitive function in postmenopausal women: the women's health initiative memory study: a randomized controlled trial. JAMA 2003, 289:2663-2672.
66. Reeves D., Winter K., Kane R., Elsmore T., Bleiberg J. Anam 2001 user's manual 2002, National Cognitive Recovery Foundation.
67. Resnick S.M., Maki P.M., Rapp S.R., Espeland M.A., Brunner R., Coker L.H., et al. Effects of combination estrogen plus progestin hormone treatment on cognition and affect. J. Clin. Endocrinol. Metab. 2006, 91:1802-1810.
68. Rohsenow D.J., Tidey J.W., Miranda R., McGeary J.E., Swift R.M., Hutchison K.E., et al. Olanzapine reduces urge to smoke and nicotine withdrawal symptoms in community smokers. Exp. Clin. Psychopharmacol. 2008, 16:215-222.
69. Romieu P., Martin-Fardon R., Bowen W.D., Maurice T. Sigma 1 receptor-related neuroactive steroids modulate cocaine-induced reward. J. Neurosci. 2003, 23:3572-3576.
70. Russo S.J., Sun W.L., Minerly A.C., Weierstall K., Nazarian A., Festa E.D., et al. Progesterone attenuates cocaine-induced conditioned place preference in female rats. Brain Res. 2008, 1189:229-235.
71. Rylance P.B., Brincat M., Lafferty K., De Trafford J.C., Brincat S., Parsons V., et al. Natural progesterone and antihypertensive action. Br. Med. J. (Clin. Res. Ed.) 1985, 290:13-14.
72. Scharf D., Shiffman S. Are there gender differences in smoking cessation, with and without bupropion? Pooled- and meta-analyses of clinical trials of bupropion sr. Addiction 2004, 99:1462-1469.
73. Schussler P., Kluge M., Yassouridis A., Dresler M., Held K., Zihl J., et al. Progesterone reduces wakefulness in sleep eeg and has no effect on cognition in healthy postmenopausal women. Psychoneuroendocrinology 2008, 33:1124-1131.
74. Sherwin B.B. Sex hormones and psychological functioning in postmenopausal women. Exp. Gerontol. 1994, 29:423-430.
75. Smith S.S., Aoki C., Shen H. Puberty, steroids and gaba(a) receptor plasticity. Psychoneuroendocrinology 2009, 34(Suppl. 1):S91-S103.
76. Snively T.A., Ahijevych K.L., Bernhard L.A., Mary Ellen W. Smoking behavior, dysphoric states and the menstrual cycle: results from single smoking sessions and the natural environment. Psychoneuroendocrinology 2000, 25:677-691.
77. Sofuoglu M., Babb D.A., Hatsukami D.K. Progesterone treatment during the early follicular phase of the menstrual cycle: effects on smoking behavior in women. Pharmacol. Biochem. Behav. 2001, 69:299-304.
78. Sofuoglu M., Babb D.A., Hatsukami D.K. Effects of progesterone treatment on smoked cocaine response in women. Pharmacol. Biochem. Behav. 2002, 72:431-435.
79. Sofuoglu M., Mitchell E., Kosten T.R. Effects of progesterone treatment on cocaine responses in male and female cocaine users. Pharmacol. Biochem. Behav. 2004, 78:699-705.
80. Sofuoglu M., Mitchell E., Mooney M. Progesterone effects on subjective and physiological responses to intravenous nicotine in male and female smokers. Hum. Psychopharmacol. 2009, 24:559-564.
81. Sofuoglu M., Poling J., Gonzalez G., Gonsai K., Oliveto A., Kosten T.R. Progesterone effects on cocaine use in male cocaine users maintained on methadone: a randomized, double-blind, pilot study. Exp. Clin. Psychopharmacol. 2007, 15:453-460.
82. Solis-Ortiz S., Corsi-Cabrera M. Sustained attention is favored by progesterone during early luteal phase and visuo-spatial memory by estrogens during ovulatory phase in young women. Psychoneuroendocrinology 2008, 33:989-998.
83. Stein D.G. Progesterone exerts neuroprotective effects after brain injury. Brain Res. Rev. 2008, 57:386-397.
84. Steinberg J.L., Cherek D.R. Menstrual cycle and cigarette smoking behavior. Addict. Behav. 1989, 14:173-179.
85. Tidey J.W., Rohsenow D.J. Intention to quit moderates the effect of bupropion on smoking urge. Nicotine Tob. Res. 2009, 11:308-312.
86. Tiffany S.T., Drobes D.J. The development and initial validation of a questionnaire on smoking urges. Br. J. Addict. 1991, 86:1467-1476.
87. Tollan A., Oian P., Kjeldsen S.E., Eide I., Maltau J.M. Progesterone reduces sympathetic tone without changing blood pressure or fluid balance in men. Gynecol. Obstet. Invest. 1993, 36:234-238.
88. van Wingen G., van Broekhoven F., Verkes R.J., Petersson K.M., Backstrom T., Buitelaar J., et al. How progesterone impairs memory for biologically salient stimuli in healthy young women. J. Neurosci. 2007, 27:11416-11423.
89. Watson D., Clark L.A., Tellegen A. Development and validation of brief measures of positive and negative affect: the panas scales. J. Pers. Soc. Psychol. 1988, 54:1063-1070.
90. Woolley C.S., McEwen B.S. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J. Comp. Neurol. 1993, 336:293-306.
91. Wu F.S., Yu H.M., Tsai J.J. Mechanism underlying potentiation by progesterone of the kainate-induced current in cultured neurons. Brain Res. 1998, 779:354-358.
92. Zumoff B., Miller L., Levin J., Levit C.D., Miller E.H., Heinz U., et al. Follicular-phase serum progesterone levels of nonsmoking women do not differ from the levels of nonsmoking men. Steroids 1990, 55:557-559.