Effects of inhibitory GABA-active neurosteroids on cocaine seeking and cocaine taking in rats

Psychopharmacology

Volumn 231, Issue 17, 2014, Pages 3391-3400

  Schmoutz, Christopher D ^a   Runyon, Scott P ^b   Goeders, Nicholas E ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b RTI INTERNATIONAL   (United States)

Author keywords

Addiction; Cocaine; Drug abuse; GABA receptor; Neuroendocrine axis; Neurosteroid; Psychostimulant; Reinforcement; Relapse; Self administration

Indexed keywords

3ALPHA HYDROXY 3BETA METHYL 17BETA NITRO 5ALPHA ANDROSTANE; 3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; 4 AMINOBUTYRIC ACID; COCAINE; NEUROSTEROID; R 6305 7; UNCLASSIFIED DRUG; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; GABAERGIC RECEPTOR AFFECTING AGENT;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; BEHAVIOR CHANGE; COCAINE DEPENDENCE; CONTROLLED STUDY; DRUG DOSE COMPARISON; DRUG EFFECT; DRUG EFFICACY; DRUG SELECTIVITY; DRUG TOLERABILITY; MALE; NONHUMAN; OPERANT BEHAVIORAL TEST; PRIORITY JOURNAL; RAT; REINFORCEMENT; RELAPSE; ANIMAL; COCAINE-RELATED DISORDERS; DRUG EFFECTS; DRUG SEEKING BEHAVIOR; DRUG SELF ADMINISTRATION; FEEDING BEHAVIOR; PSYCHOLOGY; WISTAR RAT;

ANIMALS; COCAINE; COCAINE-RELATED DISORDERS; CUES; DRUG-SEEKING BEHAVIOR; EXTINCTION, PSYCHOLOGICAL; FEEDING BEHAVIOR; GABA AGENTS; MALE; NEUROTRANSMITTER AGENTS; RATS; RATS, WISTAR; SELF ADMINISTRATION;

EID: 84906939671     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-013-3404-2     Document Type: Article

References (86)

1. Agís-Balboa RC, Pinna G, Zhubi A et al (2006) Characterization of brain neurons that express enzymes mediating neurosteroid biosynthesis. Proc Natl Acad Sci U S A 103:14602-14607 (Pubitemid 44484796)
2. Akwa Y, Purdy RH, Koob GF, Britton KT (1999) The amygdala mediates the anxiolytic-like effect of the neurosteroid allopregnanolone in rat. Behav Brain Res 106:119-125 (Pubitemid 29528492)
3. Andréen L, Nyberg S, Turkmen S et al (2009) Sex steroid induced negative mood may be explained by the paradoxical effect mediated by GABAA modulators. Psychoneuroendocrinology 34:1121-1132
4. Anker JJ, Carroll ME (2010) Sex differences in the effects of allopregnanolone on yohimbine-induced reinstatement of cocaine seeking in rats. Drug Alcohol Depend 107:264-267
5. Anker JJ, Larson EB, Gliddon LA, Carroll ME (2007) Effects of progesterone on the reinstatement of cocaine-seeking behavior in female rats. Exp Clin Psychopharmacol 15:472-480 (Pubitemid 350102234)
6. Anker JJ, Holtz NA, Zlebnik N, Carroll ME (2009) Effects of allopregnanolone on the reinstatement of cocaine-seeking behavior in male and female rats. Psychopharmacology 203:63-72
7. Bäckström T, Haage D, Löfgren M et al (2011) Paradoxical effects of GABA-A modulators may explain sex steroid induced negative mood symptoms in some persons. Neuroscience 191:46-54
8. Barker JL, Harrison NL, Lange GD, Owen DG (1987) Potentiation of gamma-aminobutyric-acid-activated chloride conductance by a steroid anaesthetic in cultured rat spinal neurones. J Physiol 386:485-501 (Pubitemid 17059731)
9. Barrett AC, Negus SS, Mello NK, Caine SB (2005) Effect of GABA agonists and GABA-A receptor modulators on cocaine- and food-maintained responding and cocaine discrimination in rats. J Pharmacol Exp Ther 315(2):858-871 (Pubitemid 41500752)
10. Bianchi MT, Haas KF, Macdonald RL (2002) Alpha1 and alpha6 subunits specify distinct desensitization, deactivation and neurosteroid modulation of GABA(A) receptors containing the delta subunit. Neuropharmacology 43(4):492-502 (Pubitemid 35279561)
11. Bitran D, Hilvers RJ, Kellogg CK (1991) Anxiolytic effects of 3 alpha-hydroxy-5 alpha[beta]-pregnan-20-one: endogenous metabolites of progesterone that are active at the GABAA receptor. Brain Res 561(1):157-161
12. Campbell UC, Carroll ME (2001) Effects of ketoconazole on the acquisition of intravenous cocaine self-administration under different feeding conditions in rats. Psychopharmacology 154(3):311-318 (Pubitemid 32247192)
13. Carroll ME, Meisch RA (1981) Determinants of increased drug self-administration due to food deprivation. Psychopharmacology 74(3):197-200 (Pubitemid 11034570)
14. Carter RB, Wood PL, Wieland S et al (1997) Characterization of the anticonvulsant properties of ganaxolone (CCD 1042; 3alpha-hydroxy-3beta-methyl- 5alpha-pregnan-20-one), a selective, high-affinity, steroid modulator of the gamma-aminobutyric acid(A) receptor. J Pharmacol Exp Ther 280:1284-1295 (Pubitemid 27166725)
15. Crawley JN, Glowa JR, Majewska MD, Paul SM (1986) Anxiolytic activity of an endogenous adrenal steroid. Brain Res 398:382-385 (Pubitemid 17210185)
16. Deo GS, Dandekar MP, Upadhya MA et al (2010) Neuropeptide Y Y1 receptors in the central nucleus of amygdala mediate the anxiolytic-like effect of allopregnanolone in mice: behavioral and immunocytochemical evidences. Brain Res 1318:77-86
17. Engin E, Treit D (2007) The anxiolytic-like effects of allopregnanolone vary as a function of intracerebral microinfusion site: the amygdala, medial prefrontal cortex, or hippocampus. Behav Pharmacol 18: 461-470 (Pubitemid 47356372)
18. Feltenstein MW, See RE (2007) Plasma progesterone levels and cocaine-seeking in freely cycling female rats across the estrous cycle. Drug Alcohol Depend 89(2-3):183-189 (Pubitemid 46754668)
19. Festa ED, Jenab S, Chin J, Gazi FM, Wu HB, Russo SJ, Quinones-Jenab V (2003) Frequency of cocaine administration affects behavioral and endocrine responses in male and female Fischer rats. Cell Mol Biol (Noisy-le-grand) 49(8):1275-1280
20. Finn DA, Roberts AJ, Long S et al (2003) Neurosteroid consumption has anxiolytic effects in mice. Pharmacol Biochem Behav 76:451-462 (Pubitemid 37487901)
21. Fox HC, Hong K-IA, Siedlarz K, Sinha R (2008) Enhanced sensitivity to stress and drug/alcohol craving in abstinent cocaine-dependent individuals compared to social drinkers. Neuropsychopharmacology 33:796-805 (Pubitemid 351252705)
22. Frye CA (2007) Progestins influence motivation, reward, conditioning, stress, and/or response to drugs of abuse. Pharmacol Biochem Behav 86(2):209-219, Review
23. Fuchs RA, Evans KA, Mehta RH et al (2005) Influence of sex and estrous cyclicity on conditioned cue-induced reinstatement of cocaine-seeking behavior in rats. Psychopharmacology 179:662-672 (Pubitemid 40674768)
24. Fuchs RA, Feltenstein MW, See RE (2006) The role of the basolateral amygdala in stimulus-reward memory and extinction memory consolidation and in subsequent conditioned cued reinstatement of cocaine seeking. Eur J Neurosci 23:2809-2813 (Pubitemid 43801473)
25. Gabriele A, See RE (2010) Reversible inactivation of the basolateral amygdala, but not the dorsolateral caudate putamen, attenuates consolidation of cocaine-cue associative learning in a reinstatement model of drug-seeking. Eur J Neurosci 32:1024-1029
26. Goeders NE, Guerin GF (2008) Effects of the combination of metyrapone and oxazepam on cocaine and food self-administration in rats. Pharmacol Biochem Behav 91:181-189
27. Goeders NE, Ikemoto S, Dorairaj NR, Simpson ST, Guerin GF (1997) Effects of initial exposure to saline in rats trained under a multiple schedule of food reinforcement and cocaine self-administration. Neurosci Abstr 23:1095
28. Goeders NE, Clampitt DM, Keller C et al (2009) Alprazolam and oxazepam block the cue-induced reinstatement of extinguished cocaine seeking in rats. Psychopharmacology 201:581-588
29. Grobin AC, VanDoren MJ, Porrino LJ, Morrow AL (2005) Cortical 3 alpha-hydroxy-5 alpha-pregnan-20-one levels after acute administration of Delta 9-tetrahydrocannabinol, cocaine and morphine. Psychopharmacology 179:544-550 (Pubitemid 40674755)
30. Gulacsi A, Lee CR, Sík A, Viitanen T, Kaila K, Tepper JM, Freund TF (2003) Cell type-specific differences in chloride-regulatory mechanisms and GABA(A) receptor-mediated inhibition in rat substantia nigra. J Neurosci 23(23):8237-8246 (Pubitemid 37129640)
31. Hirani K, Sharma AN, Jain NS et al (2005) Evaluation of GABAergic neuroactive steroid 3alpha-hydroxy-5alpha-pregnane-20-one as a neurobiological substrate for the anti-anxiety effect of ethanol in rats. Psychopharmacology 180:267-278 (Pubitemid 40909672)
32. Jackson LR, Robinson TE, Becker JB (2006) Sex differences and hormonal influences on acquisition of cocaine self-administration in rats. Neuropsychopharmacology 31(1):129-138 (Pubitemid 43250948)
33. Jaworska-Feil L (1998) Opposite effects of inhibitory and excitatory neurosteroids on dopamine release from rat nucleus accumbens. Pol J Pharmacol 50:449-452
34. Kalivas PW (2007) Neurobiology of cocaine addiction: implications for new pharmacotherapy. Am J Addict 16(2):71-78, Review
35. Kaminski RM, Gasior M, Carter RB, Witkin JM (2003) Protective efficacy of neuroactive steroids against cocaine kindled-seizures in mice. Eur J Pharmacol 474(2-3):217-222 (Pubitemid 37281452)
36. Keller CM, Cornett EM, Guerin GF, Goeders NE (2013) Combinations of oxazepam and metyrapone attenuate cocaine and methamphetamine cue reactivity. Drug Alcohol Depend 133(2):405-412
37. Kerstetter KA, Aguilar VR, Parrish AB, Kippin TE (2008) Protracted time-dependent increases in cocaine-seeking behavior during cocaine withdrawal in female relative to male rats. Psychopharmacol (Berl) 198:63-75
38. Kippin TE, Fuchs RA, Mehta RH, Case JM, Parker MP, Bimonte-Nelson HA, See RE (2005) Potentiation of cocaine-primed reinstatement of drug seeking in female rats during estrus. Psychopharmacol (Berl) 182(2):245-252 (Pubitemid 41464617)
39. Lan NC, Bolger MB, Gee KW (1991) Identification and characterization of a pregnane steroid recognition site that is functionally coupled to an expressed GABAA receptor. Neurochem Res 16:347-356
40. Larson EB, Anker JJ, Gliddon LA, Fons KS, Carroll ME (2007) Effects of estrogen and progesterone on the escalation of cocaine self-administration in female rats during extended access. Exp Clin Psychopharmacol 15(5):461-471 (Pubitemid 350102233)
41. Lee JLC, Milton AL, Everitt BJ (2006) Cue-induced cocaine seeking and relapse are reduced by disruption of drug memory reconsolidation. J Neurosci 26:5881-5887 (Pubitemid 44318352)
42. Leśkiewicz M, Budziszewska B, Jaworska-Feil L, Kubera M, Basta-Kaim A, Lasoń W (2003) Inhibitory effect of some neuroactive steroids on cocaine-induced kindling in mice. Pol J Pharmacol 55(6):1131-1136
43. Lynch WJ (2008) Acquisition and maintenance of cocaine self-administration in adolescent rats: effects of sex and gonadal hormones. Psychopharmacol (Berl) 197(2):237-246
44. Lynch WJ, Carroll ME (1999) Sex differences in the acquisition of intravenously self-administered cocaine and heroin in rats. Psychopharmacol (Berl) 144(1):77-82 (Pubitemid 29242673)
45. Mellon SH, Griffin LD, Compagnone NA (2001) Biosynthesis and action of neurosteroids. Brain Res Rev 37:3-12 (Pubitemid 34020717)
46. Motzo C, Porceddu ML, Maira G et al (1996) Inhibition of basal and stress-induced dopamine release in the cerebral cortex and nucleus accumbens of freely moving rats by the neurosteroid allopregnanolone. J Psychopharmacol 10:266-272 (Pubitemid 27045921)
47. Negus SS, Mello NK, Fivel PA (2000) Effects of GABA agonists and GABA-A receptor modulators on cocaine discrimination in rhesus monkeys. Psychopharmacol (Berl) 152(4):398-407
48. Niyomchai T, Jenab S, Festa ED, Akhavan A, Quiñones-Jenab V (2006) Effects of short- and long-term estrogen and progesterone replacement on behavioral responses and c-fos mRNA levels in female rats after acute cocaine administration. Brain Res 1126(1):193-199 (Pubitemid 44895535)
49. Peltier RL, Guerin GF, Dorairaj N, Goeders NE (2001) Effects of saline substitution on responding and plasma corticosterone in rats trained to self-administer different doses of cocaine. J Pharmacol Exp Ther 299(1):114-120 (Pubitemid 32905125)
50. Peris J (1996) Repeated cocaine injections decrease the function of striatal gamma-aminobutyric acid(A) receptors. J Pharmacol Exp Ther 276(3):1002-1008
51. Perrotti LI, Russo SJ, Fletcher H, Chin J, Webb T, Jenab S, Quiñones-Jenab V (2001) Ovarian hormones modulate cocaine-induced locomotor and stereotypic activity. Ann N YAcad Sci 937:202-216 (Pubitemid 32613887)
52. Pillai GV, Smith AJ, Hunt PA, Simpson PB (2004) Multiple structural features of steroids mediate subtype-selective effects on human alpha4beta3delta GABAA receptors. Biochem Pharmacol 68(5):819-831 (Pubitemid 39044511)
53. Quinones-Jenab V, Jenab S (2010) Progesterone attenuates cocaine-induced responses. Horm Behav 58(1):22-32
54. Quinones-Jenab V, Perrotti LI, Mc Monagle J, Ho A, Kreek MJ (2000) Ovarian hormone replacement affects cocaine-induced behaviors in ovariectomized female rats. Pharmacol Biochem Behav 67(3):417-422 (Pubitemid 32103548)
55. Quinones-Jenab V, Minerly ACE, Niyomchia T et al (2008) Progesterone and allopregnanolone are induced by cocaine in serum and brain tissues of male and female rats. Pharmacol Biochem Behav 89:292-297
56. Quinton MS, Gerak LR, Moerschbaecher JM, Winsauer PJ (2006) Effects of pregnanolone in rats discriminating cocaine. Pharmacol Biochem Behav 85:385-392 (Pubitemid 44881079)
57. Reddy DS, Rogawski MA (2002) Stress-induced deoxycorticosterone-derived neurosteroids modulate GABA(A) receptor function and seizure susceptibility. J Neurosci 22(9):3795-3805 (Pubitemid 37465784)
58. Roberts DC, Koob GF (1982) Disruption of cocaine self-administration following 6-hydroxydopamine lesions of the ventral tegmental area in rats. Pharmacol Biochem Behav 17(5):901-904 (Pubitemid 13208458)
59. Roberts DC, Koob GF, Klonoff P, Fibiger HC (1980) Extinction and recovery of cocaine self-administration following 6-hydroxydopamine lesions of the nucleus accumbens. Pharmacol Biochem Behav 12(5):781-787 (Pubitemid 10045728)
60. Roberts DC, Bennett SA, Vickers GJ (1989) The estrous cycle affects cocaine self-administration on a progressive ratio schedule in rats. Psychopharmacol (Berl) 98(3):408-411 (Pubitemid 19162433)
61. Rodgers RJ, Johnson NJ (1998) Behaviorally selective effects of neuroactive steroids on plus-maze anxiety in mice. Pharmacol Biochem Behav 59(1):221-232 (Pubitemid 28053702)
62. Romieu P, Martin-Fardon R, Bowen WD, Maurice T (2003) Sigma 1 receptor-related neuroactive steroids modulate cocaine-induced reward. J Neurosci 23:3572-3576 (Pubitemid 36958464)
63. Romieu P, Lucas M, Maurice T (2006) Sigma1 receptor ligands and related neuroactive steroids interfere with the cocaine-induced state of memory. Neuropsychopharmacology 31:1431-1443
64. Roth ME, Carroll ME (2004) Sex differences in the escalation of intravenous cocaine intake following long- or short-access to cocaine self-administration. Pharmacol Biochem Behav 78(2):199-207 (Pubitemid 38829354)
65. Runyon SP, Orr M, Navarro HA et al (2009) 17beta-Nitro-5alpha-androstan- 3alpha-ol and its 3beta-methyl derivative: neurosteroid analogs with potent anticonvulsant and anxiolytic activities. Eur J Pharmacol 617:68-73
66. Rupprecht R (2003) Neuroactive steroids: mechanisms of action and neuropsychopharmacological properties. Psychoneuroendocrinology 28:139-168
67. Rupprecht R, Holsboer F (1999) Neuroactive steroids: mechanisms of action and neuropsychopharmacological perspectives. Trends Neurosci 22:410-416 (Pubitemid 29453646)
68. Russo SJ, Festa ED, Fabian SJ, Gazi FM, Kraish M, Jenab S, Quiñones-Jenab V (2003) Gonadal hormones differentially modulate cocaine-induced conditioned place preference in male and female rats. Neuroscience 120(2):523-533 (Pubitemid 37288786)
69. See RE (2002) Neural substrates of conditioned-cued relapse to drug-seeking behavior. Pharmacol Biochem Behav 71(3):517-529
70. Shen H, Gong QH, Aoki C et al (2007) Reversal of neurosteroid effects at alpha4beta2delta GABAA receptors triggers anxiety at puberty. Nat Neurosci 10:469-477 (Pubitemid 46494589)
71. Shirayama Y, Muneoka K, Fukumoto M et al (2011) Infusions of allopregnanolone into the hippocampus and amygdala, but not into the nucleus accumbens and medial prefrontal cortex, produce antidepressant effects on the learned helplessness rats. Hippocampus 21:1105-1113
72. Sinha R, Talih M, Malison R et al (2003) Hypothalamic-pituitary-adrenal axis and sympatho-adreno-medullary responses during stress-induced and drug cue-induced cocaine craving states. Psychopharmacology 170:62-72 (Pubitemid 37372479)
73. Sinha R, Garcia M, Paliwal P et al (2006) Stress-induced cocaine craving and hypothalamic-pituitary-adrenal responses are predictive of cocaine relapse outcomes. Arch Gen Psychiatry 63:324-331 (Pubitemid 43345357)
74. Smith SS (1994) Female sex steroid hormones: from receptors to networks to performance - actions on the sensorimotor system. Prog Neurobiol 44(1):55-86, Review
75. Sofuoglu M, Kosten TR (2006) Emerging pharmacological strategies in the fight against cocaine addiction. Expert Opin Emerg Drugs 11(1):91-98, Review
76. Sundström I, Bäckström T, Wang M et al (1999) Premenstrual syndrome, neuroactive steroids and the brain. Gynecol Endocrinol Off J Int Soc Gynecol Endocrinol 13:206-220 (Pubitemid 29313221)
77. Ugale RR, Sharma AN, Kokare DM et al (2007) Neurosteroid allopregnanolone mediates anxiolytic effect of etifoxine in rats. Brain Res 1184:193-201 (Pubitemid 350160573)
78. Uzunova V, Ceci M, Kohler C et al (2003) Region-specific dysregulation of allopregnanolone brain content in the olfactory bulbectomized rat model of depression. Brain Res 976:1-8 (Pubitemid 36588530)
79. Vanover KE, Suruki M, Huber M, Wilent WB, Carter RB (2000) Neuroactive steroids attenuate cocaine-induced sucrose intake in rats, but not cocaine-induced hyperactivity in mice. Psychopharmacol (Berl) 149(3):269-276 (Pubitemid 30262341)
80. Vocci F, Ling W (2005) Medications development: successes and challenges. Pharmacol Ther 108(1):94-108 (Pubitemid 41377122)
81. Volkow ND, Wang G-J, Telang F et al (2006) Cocaine cues and dopamine in dorsal striatum: mechanism of craving in cocaine addiction. J Neurosci 26:6583-6588 (Pubitemid 44318339)
82. Wang C, Marx CE, Morrow AL et al (2007) Neurosteroid modulation of GABAergic neurotransmission in the central amygdala: a role for NMDA receptors. Neurosci Lett 415:118-123 (Pubitemid 46386326)
83. Weerts EM, Froestl W, Griffiths RR (2005) Effects of GABAergic modulators on food and cocaine self-administration in baboons. Drug Alcohol Depend 80(3):369-376 (Pubitemid 41660858)
84. Wieland S, Lan NC, Mirasedeghi S, Gee KW (1991) Anxiolytic activity of the progesterone metabolite 5 alpha-pregnan-3 alpha-o1-20-one. Brain Res 565(2):263-268
85. Wieland S, Belluzzi JD, Stein L, Lan NC (1995) Comparative behavioral characterization of the neuroactive steroids 3 alpha-OH,5 alpha-pregnan-20-one and 3 alpha-OH,5 beta-pregnan-20-one in rodents. Psychopharmacology 118:65-71
86. Wilson MA, Biscardi R (1997) Influence of gender and brain region on neurosteroid modulation of GABA responses in rats. Life Sci 60:1679-1691 (Pubitemid 27210122)