Behavioral sensitization to cocaine: Cooperation between glucocorticoids and epinephrine

Psychopharmacology

Volumn 204, Issue 4, 2009, Pages 693-703

  De Jong, Inge E M ^a,b   Steenbergen, Peter J ^a   De Kloet, E Ronald ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b H LUNDBECK A S   (Denmark)

Author keywords

Adrenalectomy; Brain; Corticosterone; HPA axis; Locomotion; Psychostimulant; Stress; Sympathetic nervous system

Indexed keywords

ADRENALIN; COCAINE; CORTICOSTERONE;

ADRENALECTOMY; ADRENERGIC SYSTEM; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DBA 2 MOUSE; DRUG SENSITIZATION; HORMONE ACTION; HORMONE SUBSTITUTION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LOCOMOTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ADRENALECTOMY; ANIMALS; BEHAVIOR, ANIMAL; COCAINE; CORTICOSTERONE; DOPAMINE UPTAKE INHIBITORS; EPINEPHRINE; MALE; MICE; MICE, INBRED DBA; MOTOR ACTIVITY; SYMPATHETIC NERVOUS SYSTEM;

EID: 67349223534     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-009-1498-3     Document Type: Article

References (76)

1. A Badiani TE Robinson 2004 Drug-induced neurobehavioral plasticity: the role of environmental context Behav Pharmacol 15 327 339 (Pubitemid 39238343)
2. A Badiani MI Morano H Akil TE Robinson 1995 Circulating adrenal hormones are not necessary for the development of sensitization to the psychomotor activating effects of amphetamine Brain Res 673 13 24
3. G Blanc F Trovero P Vezina D Herve AM Godeheu J Glowinski JP Tassin 1994 Blockade of prefronto-cortical alpha 1-adrenergic receptors prevents locomotor hyperactivity induced by subcortical d-amphetamine injection Eur J Neurosci 6 293 298
4. J Borrell ER De Kloet DH Versteeg B Bohus 1983 Inhibitory avoidance deficit following short-term adrenalectomy in the rat: the role of adrenal catecholamines Behav Neural Biol 39 241 258 (Pubitemid 14186528)
5. J Borrell ER De Kloet B Bohus 1984 Corticosterone decreases the efficacy of adrenaline to affect passive avoidance retention of adrenalectomized rats Life Sci 34 99 104
6. S Cabib C Orsini M Le Moal PV Piazza 2000 Abolition and reversal of strain differences in behavioral responses to drugs of abuse after a brief experience Science 289 463 465 (Pubitemid 30490460)
7. CC Chiueh IJ Kopin 1978 Centrally mediated release by cocaine of endogenous epinephrine and norepinephrine from the sympathoadrenal medullary system of unanesthetized rats J Pharmacol Exp Ther 205 148 154 (Pubitemid 8346949)
8. L Darracq G Blanc J Glowinski JP Tassin 1998 Importance of the noradrenaline-dopamine coupling in the locomotor activating effects of d-amphetamine J Neurosci 18 2729 2739 (Pubitemid 28141818)
9. IEM De Jong ER De Kloet 2004 Glucocorticoids and vulnerability to psychostimulant drugs: toward substrate and mechanism Ann N Y Acad Sci 1018 192 198 (Pubitemid 38951406)
10. IEM De Jong ER De Kloet 2009 Critical time-window for the actions of adrenal glucocorticoids in behavioural sensitisation to cocaine Eur J Pharmacol 604 66 73
11. IEM De Jong MS Oitzl ER de Kloet 2007 Adrenalectomy prevents behavioural sensitisation of mice to cocaine in a genotype-dependent manner Behav Brain Res 177 329 339 (Pubitemid 46149901)
12. ER De Kloet M Joels F Holsboer 2005 Stress and the brain: from adaptation to disease Nat Rev Neurosci 6 463 475 (Pubitemid 40769171)
13. A Der-Avakian ST Bland MJ Schmid LR Watkins RL Spencer SF Maier 2006 The role of glucocorticoids in the uncontrollable stress-induced potentiation of nucleus accumbens shell dopamine and conditioned place preference responses to morphine Psychoneuroendocrinology 31 653 663
14. V Deroche M Marinelli S Maccari M Le Moal H Simon PV Piazza 1995 Stress-induced sensitization and glucocorticoids. I. Sensitization of dopamine-dependent locomotor effects of amphetamine and morphine depends on stress-induced corticosterone secretion J Neurosci 15 7181 7188 (Pubitemid 3010056)
15. V Deroche-Gamonet I Sillaber B Aouizerate R Izawa M Jaber S Ghozland C Kellendonk M Le Moal R Spanagel G Schutz F Tronche PV Piazza 2003 The glucocorticoid receptor as a potential target to reduce cocaine abuse J Neurosci 23 4785 4790 (Pubitemid 36706207)
16. C Drouin G Blanc AS Villegier J Glowinski JP Tassin 2002 Critical role of alpha1-adrenergic receptors in acute and sensitized locomotor effects of D-amphetamine, cocaine, and GBR 12783: influence of preexposure conditions and pharmacological characteristics Synapse 43 51 61 (Pubitemid 33115667)
17. C Drouin L Darracq F Trovero G Blanc J Glowinski S Cotecchia JP Tassin 2002 Alpha1b-adrenergic receptors control locomotor and rewarding effects of psychostimulants and opiates J Neurosci 22 2873 2884 (Pubitemid 37465836)
18. S Erb PK Hitchcott H Rajabi D Mueller Y Shaham J Stewart 2000 Alpha-2 adrenergic receptor agonists block stress-induced reinstatement of cocaine seeking Neuropsychopharmacology 23 138 150 (Pubitemid 30406898)
19. SB Floresco CL Todd AA Grace 2001 Glutamatergic afferents from the hippocampus to the nucleus accumbens regulate activity of ventral tegmental area dopamine neurons J Neurosci 21 4915 4922 (Pubitemid 32565650)
20. SM Florin R Kuczenski RS Segal 1994 Regional extracellular norepinephrine responses to amphetamine and cocaine and effects of clonidine pretreatment Brain Res 654 53 62 (Pubitemid 24259401)
21. K Fuxe AC Wikstrom S Okret LF Agnati A Harfstrand ZY Yu L Granholm M Zoli W Vale Gustafsson 1985 Mapping of glucocorticoid receptor immunoreactive neurons in the rat tel- and diencephalon using a monoclonal antibody against rat liver glucocorticoid receptor Endocrinology 117 1803 1812 (Pubitemid 16200767)
22. GD Gamaro JD Denardin Jr. MB Michalowski D Catelli JB Correa MH Xavier C Dalmaz 1997 Epinephrine effects on memory are not dependent on hepatic glucose release Neurobiol Learn Mem 68 221 229 (Pubitemid 27506319)
23. NE Goeders 2002 The HPA axis and cocaine reinforcement Psychoneuroendocrinology 27 13 33 (Pubitemid 34028156)
24. NE Goeders 2003 The impact of stress on addiction Eur Neuropsychopharmacol 13 435 441 (Pubitemid 37433963)
25. NE Goeders GF Guerin 1994 Non-contingent electric footshock facilitates the acquisition of intravenous cocaine self-administration in rats Psychopharmacology (Berl) 114 63 70 (Pubitemid 24150521)
26. PE Gold RB Van Buskirk 1975 Facilitation of time-dependent memory processes with posttrial epinephrine injections Behav Biol 13 145 153
27. PE Gold R van Buskirk 1978 Posttraining brain norepinephrine concentrations: correlation with retention performance of avoidance training and with peripheral epinephrine modulation of memory processing Behav Biol 23 509 520 (Pubitemid 9025146)
28. PE Gold J Vogt JL Hall 1986 Glucose effects on memory: behavioral and pharmacological characteristics Behav Neural Biol 46 145 155 (Pubitemid 16009984)
29. CN Haile T GrandPre TA Kosten 2001 Chronic unpredictable stress, but not chronic predictable stress, enhances the sensitivity to the behavioral effects of cocaine in rats Psychopharmacology (Berl) 154 213 220 (Pubitemid 32186507)
30. M Haney S Maccari M Le Moal H Simon PV Piazza 1995 Social stress increases the acquisition of cocaine self-administration in male and female rats Brain Res 698 46 52
31. A Harfstrand K Fuxe A Cintra LF Agnati I Zini AC Wikstrom S Okret ZY Yu M Goldstein H Steinbusch 1986 Glucocorticoid receptor immunoreactivity in monoaminergic neurons of rat brain Proc Natl Acad Sci USA 83 9779 9783 (Pubitemid 17223440)
32. JP Herman L Stinus M Le Moal 1984 Repeated stress increases locomotor response to amphetamine Psychopharmacology (Berl) 84 431 435 (Pubitemid 15205975)
33. JA Ihalainen H Tanila 2004 In vivo regulation of dopamine and noradrenaline release by alpha2A-adrenoceptors in the mouse nucleus accumbens J Neurochem 91 49 56 (Pubitemid 39314936)
34. R Izawa M Jaber V Deroche-Gamonet I Sillaber C Kellendonk M Le Moal F Tronche PV Piazza 2006 Gene expression regulation following behavioral sensitization to cocaine in transgenic mice lacking the glucocorticoid receptor in the brain Neuroscience 137 915 924 (Pubitemid 43053954)
35. P Kovacs I Hernadi 2003 Alpha2 antagonist yohimbine suppresses maintained firing of rat prefrontal neurons in vivo Neuroreport 14 833 836 (Pubitemid 36667921)
36. AD Le S Harding W Juzytsch D Funk Y Shaham 2005 Role of alpha-2 adrenoceptors in stress-induced reinstatement of alcohol seeking and alcohol self-administration in rats Psychopharmacology (Berl) 179 366 373
37. LB Lepsch LA Gonzalo FJ Magro R Delucia C Scavone CS Planeta 2005 Exposure to chronic stress increases the locomotor response to cocaine and the basal levels of corticosterone in adolescent rats Addict Biol 10 251 256 (Pubitemid 41309069)
38. T Lewander 1968 Effects of amphetamine on urinary and tissue catecholamines in rats after inhibition of its metabolism with desmethylimipramine Eur J Pharmacol 5 1 9
39. KC Liang RG Juler JL McGaugh 1986 Modulating effects of posttraining epinephrine on memory: involvement of the amygdala noradrenergic system Brain Res 368 125 133 (Pubitemid 16052317)
40. KC Liang LL Chen TE Huang 1995 The role of amygdala norepinephrine in memory formation: involvement in the memory enhancing effect of peripheral epinephrine Chin J Physiol 38 81 91
41. R Loy DA Koziell JD Lindsey RY Moore 1980 Noradrenergic innervation of the adult rat hippocampal formation J Comp Neurol 189 699 710 (Pubitemid 10105678)
42. JR Mantsch ES Katz 2007 Elevation of glucocorticoids is necessary but not sufficient for the escalation of cocaine self-administration by chronic electric footshock stress in rats Neuropsychopharmacology 32 367 376 (Pubitemid 46106943)
43. GJ Marek GK Aghajanian 1999 5-HT2A receptor or alpha1-adrenoceptor activation induces excitatory postsynaptic currents in layer V pyramidal cells of the medial prefrontal cortex Eur J Pharmacol 367 197 206 (Pubitemid 29106371)
44. M Marinelli PV Piazza 2002 Interaction between glucocorticoid hormones, stress and psychostimulant drugs Eur J Neurosci 16 387 394 (Pubitemid 35471854)
45. T Miyashita CL Williams 2006 Epinephrine administration increases neural impulses propagated along the vagus nerve: role of peripheral beta-adrenergic receptors Neurobiol Learn Mem 85 116 124 (Pubitemid 43247837)
46. WH Pan JC Sung SM Fuh 1996 Locally application of amphetamine into the ventral tegmental area enhances dopamine release in the nucleus accumbens and the medial prefrontal cortex through noradrenergic neurotransmission J Pharmacol Exp Ther 278 725 731 (Pubitemid 27167039)
47. WH Pan MC Hsieh HH Wu SK Lin 2007 Difference in magnitude of psychostimulant-induced extracellular norepinephrine in the ventral tegmental area contributes to discrepant prefrontal dopamine outflow Addict Biol 12 51 58 (Pubitemid 46405997)
48. JR Pauly SF Robinson AC Collins 1993 Chronic corticosterone administration enhances behavioral sensitization to amphetamine in mice Brain Res 620 195 202 (Pubitemid 23231647)
49. PV Piazza ML Le Moal 1996 Pathophysiological basis of vulnerability to drug abuse: role of an interaction between stress, glucocorticoids, and dopaminergic neurons Annu Rev Pharmacol Toxicol 36 359 378 (Pubitemid 26168703)
50. PV Piazza M Le Moal 1998 The role of stress in drug self-administration Trends Pharmacol Sci 19 67 74
51. PV Piazza JM Deminiere M Le Moal H Simon 1990 Stress- and pharmacologically-induced behavioral sensitization increases vulnerability to acquisition of amphetamine self-administration Brain Res 514 22 26 (Pubitemid 20147583)
52. RC Pierce PW Kalivas 1997 A circuitry model of the expression of behavioral sensitization to amphetamine-like psychostimulants Brain Res Brain Res Rev 25 192 216 (Pubitemid 27501800)
53. BM Prasad C Ulibarri PW Kalivas BA Sorg 1996 Effect of adrenalectomy on the initiation and expression of cocaine-induced sensitization Psychopharmacology (Berl) 125 265 273 (Pubitemid 26186183)
54. E Przegalinski M Filip J Siwanowicz E Nowak 2000 Effect of adrenalectomy and corticosterone on cocaine-induced sensitization in rats J Physiol Pharmacol 51 193 204 (Pubitemid 30436069)
55. GL Quirarte B Roozendaal JL McGaugh 1997 Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala Proc Natl Acad Sci USA 94 14048 14053 (Pubitemid 28009707)
56. JM Reul ER De Kloet 1985 Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation Endocrinology 117 2505 2511 (Pubitemid 16194083)
57. JM Rivet L Stinus M LeMoal P Mormede 1989 Behavioral sensitization to amphetamine is dependent on corticosteroid receptor activation Brain Res 498 149 153 (Pubitemid 19228173)
58. TG Robinson PM Beart 1988 Excitant amino acid projections from rat amygdala and thalamus to nucleus accumbens Brain Res Bull 20 467 471 (Pubitemid 19266440)
59. B Roozendaal 2002 Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval Neurobiol Learn Mem 78 578 595 (Pubitemid 36268680)
60. B Roozendaal O Carmi JL McGaugh 1996 Adrenocortical suppression blocks the memory-enhancing effects of amphetamine and epinephrine Proc Natl Acad Sci USA 93 1429 1433 (Pubitemid 26075139)
61. B Roozendaal S Okuda EA Van der Zee JL McGaugh 2006 Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala Proc Natl Acad Sci USA 103 6741 6746
62. L Salomon C Lanteri J Glowinski JP Tassin 2006 Behavioral sensitization to amphetamine results from an uncoupling between noradrenergic and serotonergic neurons Proc Natl Acad Sci USA 103 7476 7481 (Pubitemid 43727858)
63. ED Schmidt FJ Tilders R Binnekade AN Schoffelmeer TJ De Vries 1999 Stressor- or drug-induced sensitization of the corticosterone response is not critically involved in the long-term expression of behavioural sensitization to amphetamine Neuroscience 92 343 352 (Pubitemid 29249043)
64. ED Schmidt AN Schoffelmeer TJ De Vries G Wardeh G Dogterom JG Bol R Binnekade FJ Tilders 2001 A single administration of interleukin-1 or amphetamine induces long-lasting increases in evoked noradrenaline release in the hypothalamus and sensitization of ACTH and corticosterone responses in rats Eur J Neurosci 13 1923 1930 (Pubitemid 32537218)
65. Y Shaham D Highfield J Delfs S Leung J Stewart 2000 Clonidine blocks stress-induced reinstatement of heroin seeking in rats: an effect independent of locus coeruleus noradrenergic neurons Eur J Neurosci 12 292 302 (Pubitemid 30068434)
66. BA Sorg PW Kalivas 1991 Effects of cocaine and footshock stress on extracellular dopamine levels in the ventral striatum Brain Res 559 29 36
67. JD Steketee 2003 Neurotransmitter systems of the medial prefrontal cortex: potential role in sensitization to psychostimulants Brain Res Brain Res Rev 41 203 228 (Pubitemid 36349689)
68. DB Sternberg KR Isaacs PE Gold JL McGaugh 1985 Epinephrine facilitation of appetitive learning: attenuation with adrenergic receptor antagonists Behav Neural Biol 44 447 453 (Pubitemid 16178636)
69. JW Tidey KA Miczek 1997 Acquisition of cocaine self-administration after social stress: role of accumbens dopamine Psychopharmacology (Berl) 130 203 212 (Pubitemid 27170351)
70. M Van den Buuse M Morris C Chavez S Martin J Wang 2004 Effect of adrenalectomy and corticosterone replacement on prepulse inhibition and locomotor activity in mice Br J Pharmacol 142 543 550 (Pubitemid 38869868)
71. LJ Vanderschuren PW Kalivas 2000 Alterations in dopaminergic and glutamatergic transmission in the induction and expression of behavioral sensitization: a critical review of preclinical studies Psychopharmacology (Berl) 151 99 120 (Pubitemid 30646415)
72. LJ Vanderschuren G Wardeh TJ De Vries AH Mulder AN Schoffelmeer 1999 Opposing role of dopamine D1 and D2 receptors in modulation of rat nucleus accumbens noradrenaline release J Neurosci 19 4123 4131 (Pubitemid 29222284)
73. LJ Vanderschuren P Beemster AN Schoffelmeer 2003 On the role of noradrenaline in psychostimulant-induced psychomotor activity and sensitization Psychopharmacology (Berl) 169 176 185 (Pubitemid 37129969)
74. R Ventura S Cabib A Alcaro C Orsini S Puglisi-Allegra 2003 Norepinephrine in the prefrontal cortex is critical for amphetamine- induced reward and mesoaccumbens dopamine release J Neurosci 23 1879 1885 (Pubitemid 36321778)
75. H Weil-Malherbe J Axelrod R Tomchick 1959 Blood-brain barrier for adrenaline Science 129 1226 1227
76. CL Williams JL McGaugh 1993 Reversible lesions of the nucleus of the solitary tract attenuate the memory-modulating effects of posttraining epinephrine Behav Neurosci 107 955 962 (Pubitemid 24018205)