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Nonhuman primate models of social behavior and cocaine abuse

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Abstract

Rationale

Although cocaine is often abused in social situations, very few animal studies examine the effects of cocaine in the context of social behavior.

Objectives

This review highlights studies investigating the behavioral effects of cocaine in the context of social housing conditions using nonhuman primates. In addition, this review presents recent findings examining the effects of self-administering cocaine on social behavior and the effects of manipulations hypothesized to be stressful or enriching on the interactions between cocaine reinforcement and social rank. The following dependent variables are examined: (1) cocaine-induced changes in social behavior and (2) cocaine self-administration in cynomolgus monkeys of varying social ranks. The independent variables examined include several environmental and pharmacological manipulations.

Conclusions

The studies reviewed here indicate that several variables can differentially affect cocaine self-administration when studied in a social context, rather than in individually housed animals. These variables include the social rank and sex of the individual, drug history, the nature of the “fear”-inducing manipulation, and the reliability of cortisol as an appropriate measure of “stress.” While the inclusion of socially housed animals necessitates larger sample sizes, animal models incorporating social behavior are more homologous to the human condition and should be implemented when possible.

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References

  • Abbott DH, Keverne EB, Bercovitch FB, Shively CA, Mendoza SP, Saltzman W, Snowdon CT, Ziegler TE, Banjevic M, Garland T Jr, Sapolsky RM (2003) Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm Behav 43:67–82

    Article  PubMed  CAS  Google Scholar 

  • Adler NE, Matthews K (1993) Health physiology: why do some people get sick and some stay well? Ann Rev Psychol 45:229–259

    Article  Google Scholar 

  • Amick BC, McDonough P, Chang H, Rogers WH, Pieper CF, Duncan G (2002) Relationship between all-cause mortality and cumulative working life course psychosocial and physical exposures in the United States labor market from 1968 to 1992. Psychosom Med 64:370–381

    PubMed  Google Scholar 

  • Archie EA, Altmann J, Alberts SC (2012) Social status predicts wound healing in wild baboons. Proc Natl Acad Sci 109:9017–9022

    Article  PubMed  CAS  Google Scholar 

  • Back SE, Hartwell K, DeSantis SM, Saladin M, McRae-Clark AL, Price KL, Moran-Santa Maria MM, Baker NL, Spratt E, Kreek MJ, Brady KT (2010) Reactivity to laboratory stress provocation predicts relapse to cocaine. Drug Alcohol Depend 1–6:21–27

    Article  Google Scholar 

  • Bardo MT, Klebaur JE, Valone JM, Deaton C (2001) Environmental enrichment decreases intravenous self-administration of amphetamine in female and male rats. Psychopharmacology 155:278–284

    Article  PubMed  CAS  Google Scholar 

  • Barrett JE, Glowa JR (1977) Reinforcement and punishment of behavior by the same consequent event. Psychol Rep 40:1015–1021

    Article  Google Scholar 

  • Barrett JE, Katz JL (1981) Drug effects on behaviors maintained by different events. In: Thompson T, Dews PB, McKim WA (eds) Advances in behavioral pharmacology, vol 3. Academic, New York, pp 119–168

    Google Scholar 

  • Barrett JE, Miczek KA (1995) Behavioral techniques in preclinical neuropsychopharmacology research. In: Bloom FE, Kupfer KJ (eds) Psychopharmacology: the fourth generation of progress. Raven Press, Ltd., New York, pp 65–73

    Google Scholar 

  • Botelho S, Estanislau C, Morato S (2007) Effects of under- and overcrowding on exploratory behavior in the elevated plus-maze. Behav Processes 74:357–362

    Article  PubMed  CAS  Google Scholar 

  • Bowers CL, Crockett CM, Bowden DM (1998) Differences in stress reactivity of laboratory macaques measured by heart period and respiratory sinus arrhythmia. Am J Primatol 45:245–261

    Article  PubMed  CAS  Google Scholar 

  • Bowling SL, Rowlett JK, Bardo MT (1993) The effect of environmental enrichment on amphetamine-stimulated locomotor activity, dopamine synthesis and dopamine release. Neuropharmacology 32:885–893

    Article  PubMed  CAS  Google Scholar 

  • Bradberry CW (2000) Acute and chronic dopamine dynamics in a nonhuman primate model of recreational cocaine abuse. J Neurosci 20:7109–7115

    PubMed  CAS  Google Scholar 

  • Brown KJ, Grunberg NE (1996) Effects of environmental conditions on food consumption in female and male rats. Physiol Behav 60:293–297

    Article  PubMed  CAS  Google Scholar 

  • Brown SA, Vik PW, Patterson TL, Grant I, Shuckit MA (1995) Stress, vulnerability and adult alcohol relapse. J Stud Alcohol 56:538–545

    PubMed  CAS  Google Scholar 

  • Caldji C, Hellstrom IC, Zhang T-Y, Diorio J, Meaney MJ (2011) Environmental regulation of the neural epigenome. FEBS Lett 585:2049–2058

    Article  PubMed  CAS  Google Scholar 

  • Cameron JL (1997) Stress and behaviorally induced reproductive dysfunction in primates. Semin Reprod Endocrinol 15:37–45

    Article  PubMed  CAS  Google Scholar 

  • Cohen S, Line S, Manuck SB, Rabin BS, Heise ER, Kaplan JR (1997) Chronic stress, social status, and susceptibility to upper respiratory infections in nonhuman primates. Psychosom Med 59:213–221

    PubMed  CAS  Google Scholar 

  • Crowley TJ, Stynes AJ, Hydinger M, Kaufman IC (1974) Ethanol, methamphetamine, pentobarbital, morphine, and monkey social behavior. Arch Gen Psychiatry 31:829–838

    Article  PubMed  CAS  Google Scholar 

  • Crowley TJ, Mikulich SK, Williams EA, Zerbe GO, Ingersoll NC (1992) Cocaine, social behavior, and alcohol-solution drinking in monkeys. Drug Alcohol Depend 29:205–223

    Article  PubMed  CAS  Google Scholar 

  • Czoty PW, Nader MA (2012) Individual differences in the effects of environmental stimuli on cocaine choice in socially housed male cynomolgus monkeys. Psychopharmacology. doi:10.1007/s00213-011-2562-3

  • Czoty PW, McCabe C, Nader MA (2005) Effects of the 5-HT1A agonist (±)-8-hydroxy-2-(di-n-propylamino)tetralin (8-OH-DPAT) on cocaine choice in cynomolgus. Behav Pharmacol 16:187–191

    Article  PubMed  CAS  Google Scholar 

  • Czoty PW, Coller M, Icenhower M, Nader MA (2009a) Effects of aripiprazole and (-)NPA, dopamine D2-like receptor agonists of varying intrinsic efficacy, on cocaine vs. food choice in monkeys. FASEB J. 2009; 23 (1_MeetingAbstracts): p. 588.3

  • Czoty PW, Gould RW, Nader MA (2009b) Relationship between social rank and cortisol and testosterone concentrations in male cynomolgus monkeys (Macaca fascicularis). J Neuroendocrinol 21:68–76

    Article  PubMed  CAS  Google Scholar 

  • Czoty PW, Morgan D, Nader MA (2011) Chapter 47: group processes: social dominance. In: Decety J, Cacioppo J (eds) Handbook of social neuroscience. Oxford University Press, Inc., New York, pp 716–728

    Google Scholar 

  • Dalley JW, Fryer TD, Brichard L, Robinsin ES, Theobald DE, Laane K, Pena Y, Murphy ER, Shah Y, Probst K, Abakumova I, Aigbirhio FI, Richards HK, Hong Y, Baron JC, Everitt BJ, Robbins TW (2007) Nucleus accumbens D2/3 receptors predict trait impulsivity and cocaine reinforcement. Science 315:1267–1270

    Article  PubMed  CAS  Google Scholar 

  • Draper WA, Bernstein WS (1963) Stereotyped behaviour and cage size. Percept Mot Skills 16:231–234

    Article  Google Scholar 

  • Duncan EA, Tamashiro KLK, Nguyen MMN, Gardner SR, Woods SC, Sakai RR (2006) The impact of moderate alcohol consumption on aggression and the formation of dominance hierarchies in rats. Psychopharmacology 189:83–94

    Article  PubMed  CAS  Google Scholar 

  • Dworkin SI, Mirkis S, Smith JE (1995) Response-dependent versus response-independent presentation of cocaine: differences in the lethal effects of the drug. Psychopharmacology 117:262–266

    Article  PubMed  CAS  Google Scholar 

  • Gadek-Michalska A, Bugajski J (2003) Repeated handling, restraint, or chronic crowding impair the hypothalamic-pituitary-adrenocortical response to acute restraint stress. J Physiol Pharmacol 54:449–459

    PubMed  CAS  Google Scholar 

  • Gesquiere LR, Learn NH, Simao MC, Onyango PO, Alberts SC, Altmann J (2011) Life at the top: rank and stress in wild male baboons. Science 333:357–360

    Article  PubMed  CAS  Google Scholar 

  • Goeders NE (2002) The HPA axis and cocaine reinforcement. Psychoneuroendocrinology 27:13–33

    Article  PubMed  CAS  Google Scholar 

  • Goeders NE, Guerin GF (1994) Non-contingent electric footshock facilitates the acquisition of intravenous cocaine self-administration in rats. Psychopharmacology 114:63–70

    Article  PubMed  CAS  Google Scholar 

  • Goodman E, Huang B (2002) Socioeconomic status, depressive symptoms and adolescent substance use. Arch Pediatr Adolesc Med 156:448–453

    PubMed  Google Scholar 

  • Gould RW, Porrino LJ, Nader MA (2012) Nonhuman primate models of addiction and PET imaging: dopamine system dysregulation. Curr Top Behav Neurosci 11:25–44

    Article  PubMed  Google Scholar 

  • Goymann W, Wingfield JC (2004) Allostatic load, social status and stress hormones: the costs of social status matter. Anim Behav 67:591–602

    Article  Google Scholar 

  • Grant KA, Shively CA, Nader MA, Ehrenkaufer RL, Line SW, Morton TE, Gage HD, Mach RH (1998) Effect of social status on striatal dopamine D2 receptor binding characteristics in cynomolgus monkeys assessed with positron emission tomography. Synapse 29:80–83

    Article  PubMed  CAS  Google Scholar 

  • Green TA, Gehrke BJ, Bardo MT (2002) Environmental enrichment decreases intravenous amphetamine self-administration in rats: dose–response functions for fixed- and progressive ratio schedules. Psychopharmacology 162:373–378

    Article  PubMed  CAS  Google Scholar 

  • Hackman DA, Farah MJ, Meaney MJ (2010) Socioeconomic status and the brain: mechanistic insights from human and animal research. Nat Rev 11:651–659

    Article  CAS  Google Scholar 

  • Hall FS, Wilkinson LS, Humby T, Inglis W, Kendall DA, Marsden CA, Robbins TW (1998) Isolation rearing in rats: pre- and postsynaptic changes in striatal dopaminergic systems. Pharmacol Biochem Behav 59:859–872

    Article  PubMed  CAS  Google Scholar 

  • Henry JP, Stephens PM (1977) Stress, health and the social environment. Springer, New York

    Book  Google Scholar 

  • Higley AE, Crane NA, Spadoni AD, Queool SB, Goodell V, Mason BJ (2011) Craving in response to stress induction in a human laboratory paradigm predicts treatment outcome in alcohol-dependent individuals. Psychopharmacology 218:121–129

    Article  PubMed  CAS  Google Scholar 

  • Howell LL, Murnane KS (2011) Nonhuman primate positron emission tomography neuroimaging in drug abuse research. J Pharmacol Exp Ther 337:324–334

    Article  PubMed  CAS  Google Scholar 

  • Howell LL, Votaw JR, Goodman MM, Lindsey KP (2010) Cortical activation during cocaine use and extinction in rhesus monkeys. Psychopharmacology 208:191–199

    Article  PubMed  CAS  Google Scholar 

  • Howes SR, Dalley JW, Morrison CH, Robbins TW, Everitt BJ (2000) Leftward shift in the acquisition of cocaine self-administration in isolation-reared rats: relationship to extracellular levels of dopamine, serotonin and glutamate in the nucleus accumbens and amygdala-striatal FOS expression. Psychopharmacology 151:55–63

    Article  PubMed  CAS  Google Scholar 

  • Kalin NH, Shelton SE, Davidson RJ, Kelley AE (2001) The primate amygdala mediates acute fear but not the behavioral and physiological components of anxious temperament. J Neurosci 21:2067–2074

    PubMed  CAS  Google Scholar 

  • Kalivas PW, Duffy P (1989) Similar effects of daily cocaine and stress on mesocorticolimbic dopamine neurotransmission in the rat. Biol Psychiatry 25:913–928

    Article  PubMed  CAS  Google Scholar 

  • Kaplan JR, Manuck SB (1999) Status, stress, and atherosclerosis: the role of environment and individual behavior. Ann N Y Acad Sci 896:145–161

    Article  PubMed  CAS  Google Scholar 

  • Kaplan JR, Manuck SB, Clarkson TB, Lusso FM, Taub DM (1982) Social status, environment, and atherosclerosis in cynomolgus monkeys. Arteriosclerosis 2:359–368

    Article  PubMed  CAS  Google Scholar 

  • Kaplan JR, Adams MR, Koritnik DR, Rose JC, Manuck SB (1986) Adrenal responsiveness and social status in intact and ovariectomized Macaca fascicularis. Am J Primatol 11:181–193

    Article  CAS  Google Scholar 

  • Kaplan JR, Heise ER, Manuck SB, Shively CA, Cohen S, Rabin BS, Kasprowicz AL (1991) The relationship of agonistic and affiliative behavior patterns to cellular immune function among cynomolgus monkeys (Macaca fascicularis) living in unstable social groups. Am J Primatol 25:157–173

    Article  Google Scholar 

  • Kaplan JR, Phillips-Conroy J, Fontenot MB, Jolly CJ, Fairbanks LA, Mann JJ (1999) Cerebrospinal fluid monoaminergic metabolites differ in wild Anubis and hybrid (Anubis hamadryas) baboons: possible relationships to life history and behavior. Neuropsychopharmacology 20:517–524

    Article  PubMed  CAS  Google Scholar 

  • Kaplan JR, Chen H, Appt SE, Lees CJ, Franke AA, Berga SL et al (2010) Impairment of ovarian function and associated health-related abnormalities are attributable to low social status in premenopausal monkeys and not mitigated by a high-isoflavone soy diet. Hum Reprod 25:2083–2094

    Article  Google Scholar 

  • Katz JL, Higgins ST (2003) The validity of the reinstatement model of craving and relapse to drug use. Psychopharmacology 168:21–30

    Article  PubMed  CAS  Google Scholar 

  • Kaufman BM, Pouliot AL, Tiefenbacher S, Novak MA (2004) Short and long-term effects of a substantial change in cage size on individually housed, adult male rhesus monkeys (Macaca mulata). Appl Anim Behav Sci 88:319–330

    Article  Google Scholar 

  • Knobbout DA, Ellenbroek BA, Cools AR (1996) The influence of social structure on social isolation in amphetamine-treated Java monkeys (Macaca fascicularis). Behav Pharmacol 7:417–429

    PubMed  Google Scholar 

  • Koob G, Kreek MJ (2007) Stress, dysregulation of drug reward pathways, and the transition to drug dependence. Am J Psychiatry 164:1149–1159

    Article  PubMed  Google Scholar 

  • Kosten TA (1992) Can cocaine craving be a medication outcome?: drug craving and relapse in opioid and cocaine dependence. Am J Addict 1:230–239

    Google Scholar 

  • Krantz DS, McCeney MK (2002) Effects of psychological and social factors on organic disease: a critical assessment of research on coronary heart disease. Ann Rev Psychol 53:341–369

    Article  Google Scholar 

  • Machado CJ, Kazama AM, Bachevalier J (2009) Impact of amygdala, orbital frontal, or hippocampal lesions on threat avoidance and emotional reactivity in nonhuman primates. Emotion 9:147–163

    Article  PubMed  Google Scholar 

  • Martin SP, Smith EO, Byrd LD (1990) Effects of dominance rank on d-amphetamine-induced increases in aggression. Pharmacol Biochem Behav 37:493–496

    Article  PubMed  CAS  Google Scholar 

  • Martinez D, Broft A, Foltin RW, Slifstein M, Hwang DR, Huang Y, Perez A, Frankle WG, Cooper T, Kleber HD, Fischman MW, Laruelle M (2004) Cocaine dependence and D2 receptor availability in the functional subdivisions of the striatum: relationship with cocaine-seeking behavior. Neuropsychopharmacology 29:1190–1202

    Article  PubMed  CAS  Google Scholar 

  • Martinez D, Orlowska D, Narendran R, Slifstein M, Liu F, Kumar D, Broft A, Van Heertum R, Kleber HD (2010) Dopamine type 2/3 receptor availability in the striatum and social status in human volunteers. Biol Psychiatry 67:275–278

    Article  PubMed  CAS  Google Scholar 

  • McKenzie-Quirk SD, Miczek KA (2008) Social rank and social separation as determinants of alcohol drinking in squirrel monkeys. Psychopharmacology 201:137–145

    Article  PubMed  CAS  Google Scholar 

  • Miczek KA, de Almeida RMM (2012) The case for basic research on the psychopharmacology of aggression. J Clin Psychopharmacol 32:1–2

    Article  PubMed  Google Scholar 

  • Miczek KA, de Wit H (2008) Challenges for translational psychopharmacology research—some basic principles. Psychopharmacology 199:291–301

    Article  PubMed  CAS  Google Scholar 

  • Miczek KA, Gold LH (1983) d Amphetamine in squirrel monkeys of different social status: effects on social and agonistic behavior, locomotion, and stereotypies. Psychopharmacology 81:183–190

    Article  PubMed  CAS  Google Scholar 

  • Miczek KA, Yoshimura H (1982) Disruption of primate social behavior by d-amphetamine and cocaine: differential antagonism by antipsychotics. Psychopharmacology 76:163–171

    Article  PubMed  CAS  Google Scholar 

  • Miczek KA, Woolley J, Schlisserman S, Yoshimura H (1981) Analysis of amphetamine effects on agonistic and affiliative behavior in squirrel monkeys (Saimiri sciureus). Pharmacol Biochem Behav 14(suppl 1):103–107

    PubMed  CAS  Google Scholar 

  • Miczek KA, Winslow JT, DeBold JF (1984) Heightened aggressive behavior by animals interacting with alcohol treated conspecifics: studies with mice, rats and squirrel monkeys. Pharmacol Biochem Behav 20:349–353

    Article  PubMed  CAS  Google Scholar 

  • Miczek KA, Covington HE III, Nikulina EM Jr, Hammer RP (2004) Aggression and defeat: persistent effects on cocaine self administration and gene expression in peptidergic and aminergic mesocorticolimbic circuits. Neurosci Biobehav Rev 27:787–802

    Article  PubMed  CAS  Google Scholar 

  • Morgan D, Grant KA, Prioleau OA, Nader SH, Kaplan JR, Nader MA (2000) Predictors of social status in cynomolgus monkeys (Macaca fascicularis) after group formation. Am J Primatol 52:115–131

    Article  PubMed  CAS  Google Scholar 

  • Morgan D, Grant KA, Gage HD, Mach RH, Kaplan JR, Prioleau O, Nader SH, Buchheimer N, Ehrenkaufer RL, Nader MA (2002) Social dominance in monkeys: dopamine D2 receptors and cocaine self administration. Nat Neurosci 5:169–174

    Article  PubMed  CAS  Google Scholar 

  • Morris EK (1992) The aim, progress, and evolution of behavioral analysis. Behav Anal 15:3–29

    PubMed  CAS  Google Scholar 

  • Nader MA, Czoty PW (2005) PET imaging studies of dopamine D2 receptors in monkey models of cocaine abuse: genetic predisposition versus environmental modulation. Am J Psychiatry 162:1473–1482

    Article  PubMed  Google Scholar 

  • Nader MA, Daunais JB, Moore T, Nader SH, Moore RJ, Smith HR, Friedman DP, Porrino LJ (2002) Effects of cocaine self-administration on striatal dopamine systems in rhesus monkeys: initial and chronic exposure. Neuropsychopharmacology 27:3–46

    Article  Google Scholar 

  • Nader MA, Morgan D, Gage HD, Nader SH, Calhoun TL, Buchheimer N, Ehrenkaufer R, Mach RH (2006) PET imaging of dopamine D2 receptors during chronic cocaine self-administration in monkeys. Nat Neurosci 9:1050–1056

    Article  PubMed  CAS  Google Scholar 

  • Nader MA, Czoty PW, Gould RW, Riddick NV (2010) Characterizing organism x environment interactions in nonhuman primate models of addiction: PET imaging studies of dopamine D2 receptors. In: Robbins T, Everritt B, Nutt DJ (eds) The neurobiology of drug addiction: new vistas. Oxford University Press, Oxford, pp 187–202

    Google Scholar 

  • Nader MA, Nader SH, Czoty PW, Riddick NV, Gage HD, Gould RW, Blaylock BL, Kaplan JR, Garg PK, Davies HML, Morton D, Garg S, Reboussin BA (2012) Social dominance in female monkeys: dopamine receptor function and cocaine reinforcement. Biol Psychiatry 72:414–421

    Article  PubMed  CAS  Google Scholar 

  • Negus SS (2003) Rapid assessment of choice between cocaine and food in rhesus monkeys: effects of environmental manipulations and treatment with d-amphetamine and flupenthixol. Neuropsychopharmacology 28:919–931

    PubMed  Google Scholar 

  • Nelson EE, Shelton SE, Kalin NH (2003) Individual differences in the responses of naïve rhesus monkeys to snakes. Emotion 3:3–11

    Article  PubMed  Google Scholar 

  • Paronis CA, Gasior M, Bergman J (2002) Effects of cocaine under concurrent fixed ratio schedules of food and IV drug availability: a novel choice procedure in monkeys. Psychopharmacology 163:283–291

    Article  PubMed  CAS  Google Scholar 

  • Paulk HH, Dienske H, Ribbens LG (1977) Abnormal behavior in relation to cage size in rhesus monkeys. J Abnorm Psychol 86:87–92

    Article  PubMed  CAS  Google Scholar 

  • Prather MD, Lavenex P, Mauldin-Jourdain ML, Mason WA, Capitanio JP, Mendoza SP, Amaral DG (2001) Increased social fear and decreased fear of objects in monkeys with neonatal amygdala lesions. Neuroscience 106:653–658

    Article  PubMed  CAS  Google Scholar 

  • Preston KM, Epstein DH (2011) Stress in the daily lives of cocaine and heroin users: relationship to mood, craving, relapse triggers, and cocaine use. Psychopharmacology 218:29–37

    Article  PubMed  CAS  Google Scholar 

  • Quadros IMH, Miczek KA (2009) Two modes of intense cocaine bingeing: increased persistence after social defeat stress and increased rate of intake due to extended access conditions in rats. Psychopharmacology 206:109–120

    Article  PubMed  CAS  Google Scholar 

  • Sapolsky RM (2005) The influence of social hierarchy on primate health. Science 308:648–652

    Article  PubMed  CAS  Google Scholar 

  • Shively C, Kaplan J (1984) Effects of social factors on adrenal weight and related physiology of Macaca fascicularis. Physiol Behav 33:777–782

    Article  PubMed  CAS  Google Scholar 

  • Smith MA (2012) Peer influences on drug self-administration: social facilitation and social inhibition of cocaine intake in male rats. Psychopharmacology. doi:10.1007/s00213-012-2737-6

  • Smith EO, Byrd LD (1984) Contrasting effects of d-amphetamine on affiliation and aggression in monkeys. Pharmacol Biochem Behav 20:255–260

    Article  PubMed  CAS  Google Scholar 

  • Smith EO, Byrd LD (1985) d-Amphetamine induced changes in social interaction patterns. Pharmacol Biochem Behav 22:135–139

    Article  PubMed  CAS  Google Scholar 

  • Smith MA, Lynch WJ (2011) Exercise as a potential treatment for drug abuse: evidence from preclinical studies. Front Psychiatry 2:1–10

    Article  Google Scholar 

  • Sorg BA, Kalivas PW (1991) Effects of cocaine and footshock stress on extracellular dopamine levels in the ventral striatum. Brain Res 559:29–36

    Article  PubMed  CAS  Google Scholar 

  • Spealman RD (1979) Behavior maintained by termination of a schedule of self-administered cocaine. Science 204:1231–1233

    Article  PubMed  CAS  Google Scholar 

  • Takahashi A, Quadros IM, De Almeida RMM, Miczek KA (2012) Behavioral and pharmacogenetics of aggressive behavior. Curr Top Behav Neurosci 12:73–138

    Google Scholar 

  • Vellucci SV (1990) Primate social behavior—anxiety or depression? Pharmacol Ther 47:167–180

    Article  PubMed  CAS  Google Scholar 

  • Volkow ND, Fowler JS, Wang GJ, Hitzemann R, Logan J, Schlyer DJ, Dewey SL, Wolf AP (1993) Decreased dopamine D2 receptor availability is associated with reduced frontal metabolism in cocaine abusers. Synapse 14:169–177

    Article  PubMed  CAS  Google Scholar 

  • Volkow ND, Wang GJ, Fowler JS, Logan J, Gatley SJ, Gifford A, Hitzemann R, Ding YS, Pappas N (1999) Prediction of reinforcing responses to psychostimulants in humans by brain dopamine D2 receptor levels. Am J Psychiatry 156:1440–1443

    PubMed  CAS  Google Scholar 

  • Waldrop AE, Back SE, Brady KT, Upadhyaya HP, McRae AL, Saladin ME (2007) Daily stressor sensitivity, abuse effects, and cocaine use in cocaine dependence. Addict Behav 32:3015–3025

    Article  PubMed  Google Scholar 

  • Weerts EM, Fantegrossi WE, Goodwin AK (2007) The value of nonhuman primates in drug abuse research. Exp Clin Psychopharmacol 15:309–327

    Article  PubMed  CAS  Google Scholar 

  • Wohlfarth T, Van Den Brink W (1998) Social class and substance use diosrders: the value of social class as distinct from socioeconomic status. Soc Sci Med 47:51–58

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

Preparation of this manuscript was supported by NIDA grants R37 DA10584 and R01 DA017763. The authors thank Robert Gould, Natallia Riddick, Tonya Calhoun, Michael Coller, Mikki Sandridge, Matthew Dickens, Clifford Hubbard, Osric Prioleau, Ciara McCabe, and Michelle Icenhower for excellent technical assistance over the years and Kathleen A. Grant, Robert H. Mach, H. Donald Gage, and Jay R. Kaplan for our long-standing collaborations.

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Nader, M.A., Czoty, P.W., Nader, S.H. et al. Nonhuman primate models of social behavior and cocaine abuse. Psychopharmacology 224, 57–67 (2012). https://doi.org/10.1007/s00213-012-2843-5

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