Drug Abuse: Vulnerability and Transition to Addiction

Abstract

Intrinsic vulnerability is central to the transition of recreational drug use to misuse. Several factors contribute to vulnerability, inherent or acquired, and they account for the huge individual differences observed concerning the propensity to enter in the addiction process. Some of the multifactional causes for a vulnerable phenotype will be examined: genetic factors, age and gender influences, various comorbidities and epidemiological observations. Stress-induced vulnerability will be particularly reviewed because it provides a good model for a pathophysiological research and for relating environmental events to biological consequences of drug vulnerability, namely through the striato-cortical dopamine system. Experimental studies are generally blind concerning these historical factors that contribute vulnerability and a critical evaluation of current animal models is needed. The transition of the last stage of the process, addiction, is conceptualized as a progression from homeostasis to allostasis and then, to pathology.

References

• 1 Abi-Dargham A, Kegeles LS, Martinez D. et al . Dopamine mediation of positive reinforcing effects of amphetamine in stimulant naive healthy volunteers: results from a large cohort.  Eur Neuropsychopharmacol. 2003;  13 459-468
• 2 Adriani W, Giannakopoulou D, Bokulic Z. et al . Response to novelty, social and self-control behaviors, in rats exposed to neonatal anoxia: modulatory effects of an enriched environment.  Psychopharmacology. 2006;  184 155-165
• 3 Ahmed SH, Koob GF. Transition from moderate to excessive drug intake: Change in hedonic set point.  Science. 1998;  282 298-300
• 4 Association AP. Diagnostic and Statistical Manual of Mental Disorders. 4th Revised edition. American Psychiatric Press, Washington, DC.943. American Psychiatric Press ed 1994: 943
• 5 Angulo JA, MacEwen BS. Molecular aspects of neuropeptide regulation and function in the corpus striatum and nucleus-accumbens.  Brain Res Rev. 1994;  19 1-28
• 6 Anthony JC, Warner LA, Kessler RC. Comparative epidemiology of dependence on tobacco, alcohol, controlled substances, and inhalants: Basic findings from the National Comorbidity Survey.  Experim Clin Psychopharmacol. 1994;  2 244-268
• 7 Barnes GE, Murray RP, Patton D. et al .The Addiction-Prone Personality. In: Barnes GE, Murray RP, Patton, D, Bentler, PM, Anderson RE, eds. New York: Kluwer Academic/Plenum Publishers 2000: 326
• 8 Barrot M, Marinelli M, Abrous DN. et al . The dopaminergic hyper-responsiveness of the shell of the nucleus accumbens is hormone-dependent.  Europ J Neurosci. 2000;  12 973-979
• 9 Biglan A, Metzler CW, Wirt R. et al . Social and behavioral-factors associated with high-risk sexual among adolescents.  J Behav Med. 1990;  13 245-261
• 10 Blanc G, Herve D, Simon H. et al . Response to stress of mesocortico-frontal dopaminergic-neurons in rats after long-term isolation.  Nature. 1980;  284 265-267
• 11 Brake WG, Zhang TY, Diorio J. et al . Influence of early postnatal rearing conditions on mesocorticolimbic dopamine and behavioural responses to psychostimulants and stressors in adult rats.  Europ J Neurosci. 2004;  19 1863-1874
• 12 Brandon CL, Marinelli M, Baker LK. et al . Enhanced reactivity and vulnerability to cocaine following methylphenidate treatment in adolescent rats.  Neuropsychopharmacology. 2001;  25 651-661
• 13 Brandon CL, Marinelli M, White FJ. Adolescent exposure to methylphenidate alters the activity of rat midbrain dopamine neurons.  Biological Psychiatry. 2003;  54 1338-1344
• 14 Brodal A. Neurological Anatomy in Relation to Clinical Medicine. Oxford University Press, New York 1969
• 15 Cabib S, Orsini C, Le Moal M. et al . Abolition and reversal of strain differences in behavioral responses to drugs of abuse after a brief experience.  Science. 2000;  289 463-465
• 16 Caldji C, Tannenbaum B, Sharma S. et al . Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat.  Proc National Acad Sci US Am. 1998;  95 5335-5340
• 17 Caprioli D, Paolone G, Celentano M. et al . Environmental modulation of cocaine self-administration in the rat.  Psychopharmacology. 2007;  192 397-406
• 18 Carr KD, Kim GY, de Vaca SC. Rewarding and locomotor-activating effects of direct dopamine receptor agonists are augmented by chronic food restriction in rats.  Psychopharmacology. 2001;  154 420-428
• 19 Carroll ME, Lynch WJ, Roth ME. et al . Sex and estrogen influence drug abuse.  Trends in Pharmacological Sciences. 2004;  25 273-279
• 20 Caster JM, Walker QD, Kuhn CM. A single high dose of cocaine induces differential sensitization to specific behaviors across adolescence.  Psychopharmacology. 2007;  193 247-260
• 21 Colvis CM, Pollock JD, Goodman RH. et al . Epigenetic mechanisms and gene networks in the nervous system.  J Neurosci. 2005;  25 10379-10389
• 22 Crabbe JC. Genetic contributions to addiction.  Ann Rev Psychol. 2002;  53 435-462
• 23 Crews F, He J, Hodge C. Adolescent cortical development: A critical period of vulnerability for addiction.  Pharmacol Biochem Behav. 2007;  86 189-199
• 24 Crome IB. Gender differences in substance misuse and psychiatric comorbidity.  Curr Opin Psychiatry. 1997;  10 194-198
• 25 Dazzi L, Seu E, Cherchi G. et al . Estrous cycle-dependent changes in basal and ethanol-induced activity of cortical dopaminergic neurons in the rat.  Neuropsychopharmacology. 2007;  32 892-901
• 26 de Kloet ER. Brain corticosteroid receptor balance and homeostatic control.  Front Neuroendocrinol. 1991;  12 95-164
• 27 de Wit H, Uhlenhuth EH, Johanson CE. Individual-differences in the reinforcing and subjective effects of amphetamine and diazepam.  Drug and Alcohol Dependence. 1986;  16 341-360
• 28 Deminiere JM, Piazza PV, Guegan G. et al . Increased locomotor response to novelty and propensity to intravenous amphetamine self-administration in adult offspring of stressed mothers.  Brain Res. 1992;  586 135-139
• 29 Deroche V, Marinelli M, LeMoal M. et al . Glucocorticoids and behavioral effects of psychostimulants. 2. Cocaine intravenous self-administration and reinstatement depend on glucocorticoid levels.  J Pharmacol Experiment Therap. 1997;  281 1401-1407
• 30 Deroche-Gamonet V, Sillaber I, Aouizerate B. et al . The glucocorticoid receptor as a potential target to reduce cocaine abuse.  J Neurosci. 2003;  23 4785-4790
• 31 Deroche-Gamonet V, Belin D, Piazza PV. Evidence for addiction-like behavior in the rat.  Science. 2004;  305 1014-1017
• 32 DiFranza JR. Hooked from the first cigarette.  Scientific American. 2008;  298 82-87
• 33 Dreher JC, Schmidt PJ, Kohn P. et al . Menstrual cycle phase modulates reward-related neural function in women.  Proc Nat Acad Sci USA. 2007;  104 2465-2470
• 34 Fox HC, Hong KA, Paliwal P. et al . Altered levels of sex and stress steroid hormones assessed daily over a 28-day cycle in early abstinent cocaine-dependent females.  Psychopharmacology. 2008;  195 527-536
• 35 Fride E, Weinstock M. Alterations in behavioral and striatal dopamine asymmetries induced by prenatal stress.  Pharmacol Biochem Behav. 1989;  32 425-430
• 36 Goeders NE, Guerin GF. Noncontingent electric footshock facilitates the acquisition of intravenous cocaine self-adminstration in rats.  Psychopharmacology. 1994;  114 63-70
• 37 Goldman D, Oroszi G, Ducci F. The genetics of addictions: Uncovering the genes.  Nat Rev Genet. 2005;  6 521-532
• 38 Goodman A. Neurobiology of addiction – An integrative review.  Biochemical Pharmacology. 2008;  75 266-322
• 39 Grant BF, Dawson DA. Age of onset of drug use and its association with DSM-IV drug abuse and dependence: Results from the National Longitudinal Alcohol Epidemiologic Survey.  J Subst Abuse. 1998;  10 163-173
• 40 Grant BF, Stinson FS, Dawson DA. et al . Prevalence and co-occurrence of substance use disorders and independent mood and anxiety disorders – Results from the national epidemiologic survey on alcohol and related conditions.  Arch Gen Psychiat. 2004;  61 807-816
• 41 Grant JE, Levine L, Kim D. et al . Impulse control disorders in adult psychiatric inpatients.  Am J Psychiat. 2005;  162 2184-U2186
• 42 Hall FS. Social deprivation of neonatal, adolescent, and adult rats has distinct neurochemical and behavioral consequences.  Critical Rev Neurobiol. 1998;  12 129-162
• 43 Harfstrand A, Fuxe K, Cintra A. et al . Glucocorticoid receptor immunoreactivity in monoaminergic neurons of rat-brain.  Proc Nat Acad Sci USA. 1986;  83 9779-9783
• 44 Heidbreder CA, Weiss IC, Domeney AM. et al . Behavioral, neurochemical and endocrinological characterization of the early social isolation syndrome.  Neuroscience. 2000;  100 749-768
• 45 Henry C, Guegant G, Cador M. et al . Prenatal stress in rats facilitates amphetamine-induced sensitization and induces long-lasting changes in dopamine-receptors in the nucleus-accumbens.  Brain Research. 1995;  685 179-186
• 46 Hernandez-Avila CA, Rounsaville BJ, Kranzler HR. Opioid-, cannabis- and alcohol-dependent women show more rapid progression to substance abuse treatment.  Drug and Alcohol Dependence. 2004;  74 265-272
• 47 Hooks MS, Juncos JL, Justice JB. et al . Individual locomotor response to novelty predicts selective alterations in D-1 and D-2 receptors and messenger-RNAS.  J Neurosci. 1994;  14 6144-6152
• 48 Jirtle RL, Skinner MK. Environmental epigenomics and disease susceptibility.  Nat Rev Genet. 2007;  8 253-262
• 49 Joels M, de Kloet ER. Control of neuronal excitability by corticosteroid hormones.  Trends Neurosci. 1992;  15 25-30
• 50 Joels M, de Kloet ER. Mineralocorticoid and glucocorticoid receptors in the brain - Implications for ion permeability and transmitter systems.  Prog Neurobiol. 1994;  43 1-36
• 51 Kandel DB, Jessor R. The gateway hypothesis revisited. In: Kandel, D.B. (Ed). Stages and pathways of drugs involvement examining the gateway hypothesis. Cambridge University Press, New York 2002: 365-372
• 52 Kessler RC, Berglund P, Demler O. et al . Lifetime prevalence and age-of-onset distributions’ of DSM-IV disorders in the national comorbidity survey replication.  Arch Gen Psychiat. 2005;  62 593-602
• 53 Kessler RC, Chiu WT, Demler O. et al . Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey Replication.  Archives of General Psychiatry. 2005;  62 617-627
• 54 Khantzian EJ. The self-medication hypothesis of addictive disorders – Focus on heroin and cocaine dependence.  Am J Psychiat. 1985;  142 1259-1264
• 55 Khantzian EJ. Self-regulation and self-medication factors in alcoholism and the addictions: similarities and differences. In: Galanter M, ed Combined alcohol and other drug dependence. Plenum Press, New York 1990: 255-271
• 56 Khantzian EJ. The self-medication hypothesis of substance use disorders: A reconsideration and recent applications.  Harvard Rev Psychiat. 1997;  4 231-244
• 57 Kippin TE, Szumlinski KK, Kapasova Z. et al . Prenatal stress enhances responsiveness to cocaine.  Neuropsychopharmacology. 2008;  33 769-782
• 58 Koob GF. A role for brain stress systems in addiction.  Neuron. 2008;  59 11-34
• 59 Koob GF, LeMoal M. Drug abuse: Hedonic homeostatic dysregulation.  Science. 1997;  278 52-58
• 60 Koob GF, Le Moal M. Drug addiction, dysregulation of reward, and allostasis.  Neuropsychopharmacology. 2001;  24 97-129
• 61 Koob GF, Le Moal M. Addiction and the brain antireward system.  Ann Rev Psychol. 2008;  59 29-53
• 62 Koob GF, Le Moal M. Neurobiological mechanisms for opponent motivational processes in addiction.  Philosophical Transactions of the Royal Society B-Biological Sciences. 2008;  363 3113-3123
• 63 Koob GF, Le Moal M. Neurobiology of Addiction. Elsevier ed 2006: 490
• 64 Kosten TA, Miserendino MJD, Kehoe P. Enhanced acquisition of cocaine self-administration in adult rats with neonatal isolation stress experience.  Brain Research. 2000;  875 44-50
• 65 Kosten TA, Zhang XY, Kehoe P. Neurochemical and behavioral responses to cocaine in adult male rats with neonatal isolation experience.  J Pharmacol Experim Therap. 2005;  314 661-667
• 66 Kreek MJ, Nielsen DA, Butelman ER. et al . Genetic influences on impulsivity, risk taking, stress responsivity and vulnerability to drug abuse and addiction.  Nature Neuroscience. 2005;  8 1450-1457
• 67 Ladd CO, Huot RL, Thrivikraman KV. et al . Long-term behavioral and neuroendocrine adaptations to adverse early experience.  Prog Brain Res. 1999;  122 81-103
• 68 Larson EB, Roth ME, Anker JJ. et al . Effect of short- vs. long-term estrogen on reinstatement of cocaine-seeking behavior in female rats.  Pharmacol Biochem Behav. 2005;  82 98-108
• 69 Le Moal M, Koob GF. Drug addiction: Pathways to the disease and pathophysiological perspectives.  Europ Neuropsychopharmacology. 2007;  17 377-393
• 70 Le Moal M, Simon H. Mesocorticolimbic dopaminergic network – Functional and regulatory roles.  Physiol Rev. 1991;  71 155-234
• 71 Lemaire V, Lamarque S, Le Moal M. et al . Postnatal stimulation of the pups counteracts prenatal stress-induced deficits in hippocampal neurogenesis.  Biol Psychiat. 2006;  59 786-792
• 72 Levenson JM, Sweatt JD. Epigenetic mechanisms in memory formation.  Nat Rev Neurosci. 2005;  6 108-118
• 73 Leyton M, Boileau I, Benkelfat C. et al . Amphetamine-induced increases in extracellular dopamine, drug wanting, and novelty seeking: A PET/[C-11]raclopride study in healthy men.  Neuropsychopharmacology. 2002;  27 1027-1035
• 74 Maccari S, Piazza PV, Deminiere JM. et al . Life events-induced decrease of corticosteroid type-1 receptors is associated with reduced corticosterone feedback and enhanced vulnerability to amphetamine self-administration.  Brain Research. 1991;  547 7-12
• 75 Mantsch JR, Baker DA, Serge JP. et al . Surgical adrenalectomy with diurnal corticosterone replacement slows escalation and prevents the augmentation of cocaine-induced reinstatement in rats self-administering cocaine under long-access conditions.  Neuropsychopharmacology. 2008;  33 814-826
• 76 Mantsch JR, Saphier D, Goeders NE. Corticosterone facilitates the acquisition of cocaine self-administration in rats: Opposite effects of the type II glucocorticoid receptor agonist dexamethasone.  J Pharmacol Experim Therap. 1998;  287 72-80
• 77 Marinelli M. Dopaminergic Reward Pathways and Effects of Stress. In: al’Absi M, ed. Stress and Addiction: Biological and Psychological Mechanisms. Elsevier Ltd 2007: 41-83
• 78 MacEwen BS. Stress, adaptation, and disease: allostasis and allostatic load.  Ann New York Acad Sci. 1998;  840 33-44
• 79 McEwen BS. Allostasis and allostatic load: Implications for neuropsychopharmacology.  Neuropsychopharmacology. 2000;  22 108-124
• 80 Meaney MJ. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations.  Ann Rev Neurosci. 2001;  24 1161-1192
• 81 Merikangas KR, Mehta RL, Molnar BE. et al . Comorbidity of substance use disorders with mood and anxiety disorders: Results of the International Consortium in Psychiatric Epidemiology.  Addictive Behaviors. 1998;  23 893-907
• 82 Moyer JA, Herrenkohl LR, Jacobowitz DM. Stress during pregnancy – Effect on catecholamines in discrete brain-regions of offsprings as adults.  Brain Research. 1978;  144 173-178
• 83 Najavits LM, Weiss RD, Shaw SR. The link between substance abuse and posttraumatic stress disorder in women – A research review.  Am J Addict. 1997;  6 273-283
• 84 Nauta JH, Haymaker W. Hypothalamic nuclei and fiber connections. In: Haymaker W, Anderson E, and Nauta WJH, ed In “The Hypothalamus”. Springfield Il.: Charles C. Thomas 1969: 136-209
• 85 O’Brien CP, Ehrman RN, Ternes JM. Classical conditioning in human opioid dependence. In Goldberg SR, Stolerman IP, Eds Behavioral Analysis of Drug Dependence. Academic Press, Orlando Fl 1986: 329-356
• 86 Oswald LM, Wong DF, MacCaul M. et al . Relationships among ventral striatal dopamine release, cortisol secretion, and subjective responses to amphetamine.  Neuropsychopharmacology. 2005;  30 821-832
• 87 Piazza PV, Deroche-Gamonent V, Rouge-Pont F. et al . Vertical shifts in self-administration dose-response functions predict a drug-vulnerable phenotype predisposed to addiction.  J Neurosci. 2000;  20 4226-4232
• 88 Piazza PV, Le Moal M. Glucocorticoids as a biological substrate of reward: physiological pathophysiological implications.  Brain Res Rev. 1997;  25 359-372
• 89 Piazza PV, Le Moal M. The role of stress in drug self-administration.  Trends Pharmacol Sci. 1998;  19 67-74
• 90 Piazza PV, RougePont F, Deroche V. et al . Glucocorticoids have state-dependent stimulant effects on the mesencephalic dopaminergic transmission.  Proc Nat Acad Sci USA. 1996;  93 8716-8720
• 91 Piazza PV, Deminiere JM, Le Moal M. et al . Factors that predict individual vulnerability to amphetamine self-administration.  Science. 1989;  245 1511-1513
• 92 Piazza PV, Deroche V, Deminiere JM. et al . Corticosterone in the range of stress-induced levels possesses reinforcing properties. Implications for sensation-seeking behaviors.  Proc Nat Acad Sci US Am. 1993;  90 11738-11742
• 93 Piazza PV, Deroche V, Rouge-Pont F. et al . Behavioral and biological factors associated with individual vulnerability to psychostimulant abuse.  NIDA Res Monogr. 1998;  169 105-133
• 94 Piazza PV, Le Moal M. Pathophysiological basis of vulnerability to drug abuse: Role of an interaction between stress, glucocorticoids, and dopaminergic neurons.  Ann Rev Pharm Toxicol. 1996;  36 359-378
• 95 Piazza PV, Maccari S, Deminiere JM. et al . Corticosterone levels determine individual vulnerability to amphetamine self-administration.  Proc Nat Acad Sci USA. 1991;  88 2088-2092
• 96 Piazza PV, Rouge-Pont F, Deminiere JM. et al . Dopaminergic activity is reduced in the prefrontal cortex and increased in the nucleus-accumbens of rats predisposed to develop amphetamine self-adminstration.  Brain Research. 1991;  567 169-174
• 97 Quinones-Jenab V. Why are women from Venus and men from Mars when they abuse cocaine?.  Brain Research. 2006;  1126 200-203
• 98 Robbins TW, Everitt BJ. A role for mesencephalic dopamine in activation: commentary on Berridge (2006).  Psychopharmacology. 2007;  191 433-437
• 99 Rosenzweig MR, Bennett EL. Psychobiology of plasticity: Effects of training and experience on brain and behavior.  Behav Brain Res. 1996;  78 57-65
• 100 Rouge-Pont F, Marinelli M, Le Moal M. et al . Sress-induced sensitization and glucocorticoids. 2. Sensitization of the increase in extracellular dopamine-induced by cocaine depends on stress-induced corticosterone secretion.  J Neurosci. 1995;  15 7189-7195
• 101 Rouge-Pont F, Piazza PV, Kharouby M. et al . Higher and longer stress-induced increase in dopamine concentrations in the nucleus-accumbens of animals predisposed to amphetamine self-administration. A microdialysis study.  Brain Res. 1993;  602 169-174
• 102 Rutter M, Moffitt TE, Caspi A. Gene-environment interplay and psychopathology: multiple varieties but real effects.  J Child Psychol Psychiat. 2006;  47 226-261
• 103 Salamone JD, Correa M, Farrar A. et al . Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits.  Psychopharmacology. 2007;  191 461-482
• 104 SAMHSA . Substance Abuse and Mental Health Services Administration. Results from the 2000 National Household Survey on Drug Use. Office of Applied Studies, NHSDA Series H-13. DHHS Publication No. SMA 03–3549. Rockville, MD. In. Rockville, MD 2001
• 105 SAMHSA . Substance Abuse and Mental Health Services Administration. Results from the 2002 National Survey on Drug Use and Health: National Findings (Office of Applied Studies, NHSDA Series H-22, DHHS Publication No SMA 03-386). Rockville, MD. In 2003
• 106 Sasaki H, Matsui Y. Epigenetic events in mammalian germ-cell development: reprogramming and beyond.  Nat Rev Genet. 2008;  9 129-140
• 107 Schoffelmeer ANM, Voorn P, Jonker AJ. et al . Morphine-induced increase in D-1 receptor regulated signal transduction in rat striatal neurons and its facilitation by glucocorticoid receptor activation: Possible role in behavioral sensitization.  Neurochem Res. 1996;  21 1417-1423
• 108 Shaffer HJ, LaPlante DA, LaBrie RA. et al . Toward a syndrome model of addiction: multiple expressions, common etiology.  Harvard Rev Psychiat. 2004;  12 367-374
• 109 Shaham Y, Shalev U, Lu L. et al . The reinstatement model of drug relapse: history, methodology and major findings.  Psychopharmacology. 2003;  168 3-20
• 110 Shaham Y, Stewart J. Effects of opioid and dopamine receptor antagonists on relapse induced by stress and re-exposure to heroin in rats.  Psychopharmacology. 1996;  125 385-391
• 111 Sifneos PE. Alexithymia, clinical issues, politics and crime.  Psychotherapy and Psychosomatics. 2000;  69 113-116
• 112 Smith JK, Neill JC, Costall B. Post-weaning housing conditions influence the behavioural effects of cocaine and d-amphetamine.  Psychopharmacology. 1997;  131 23-33
• 113 Spear LP. The adolescent brain and age-related behavioral manifestations.  Neuroscience and Biobehavioral Reviews. 2000;  24 417-463
• 114 Stansfield KH, Kirstein CL. Neurochemical effects of cocaine in adolescence compared to adulthood.  Develop Brain Res. 2005;  159 119-125
• 115 Stanwood GD, Levitt P. Prenatal exposure to cocaine produces unique developmental and long-term adaptive changes in dopamine D1 receptor activity and subcellular distribution.  J Neurosci. 2007;  27 152-157
• 116 Sterling P, Eyer P. Allostasis: a new paradigm to explain arousal pathology. Fisher S, Reason J, eds. Chichester, UK: Wiley 1988: 629-649
• 117 Toga AW, Thompson PM, Sowell ER. Mapping brain maturation.  Trends Neurosci. 2006;  29 148-159
• 118 Tsankova N, Renthal W, Kumar A. et al . Epigenetic regulation in psychiatric disorders.  Nat Rev Neurosci. 2007;  8 355-367
• 119 Uhl GR, Grow RW. The burden of complex genetics in brain disorders.  Arch Gen Psychiat. 2004;  61 223-229
• 120 Vallee M, Maccari S, Dellu F. et al . Long-term effects of prenatal stress and postnatal handling on age-related glucocorticoid secretion and cognitive performance: a longitudinal study in the rat.  Europ J Neurosci. 1999;  11 2906-2916
• 121 Volkow ND, Wang GJ, Fowler JS. et al . Reinforcing effects of psychostimulants in humans are associated with increases in brain dopamine and occupancy of D-2 receptors.  J Pharmacol Experim Ther. 1999;  291 409-415
• 122 Wang B, Shaham Y, Zitzman D. et al . Cocaine experience establishes control of midbrain glutamate and dopamine by corticotropin-releasing factor: A role in stress-induced relapse to drug seeking.  J Neurosci. 2005;  25 5389-5396
• 123 Wang B, You ZB, Rice KC. et al . Stress-induced relapse to cocaine seeking: roles for the CRF2 receptor and CRF-binding protein in the ventral tegmental area of the rat.  Psychopharmacology. 2007;  193 283-294
• 124 Weaver ICG, Cervoni N, Champagne FA. et al . Epigenetic programming by maternal behavior.  Nature Neuroscience. 2004;  7 847-854
• 125 Zhou Y, Spangler R, LaForge KS. et al . Corticotropin-releasing factor and type 1 corticotropin-releasing factor receptor messenger RNAs in rat brain and pituitary during “binge”-pattern cocaine administration and chronic withdrawal.  J Pharmacol Experim Ther. 1996;  279 351-358
• 126 Zhou Y, Spangler R, Schlussman SD. et al . Alterations in hypothalamic-pituitary-adrenal axis activity and in levels of proopiomelanocortin and corticotropin-releasing hormone-receptor 1 mRNAs in the pituitary and hypothalamus of the rat during chronic ‘binge’ cocaine and withdrawal.  Brain Res. 2003;  964 187-199

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