Abstract
Rationale
Alcohol may be self-administered for its anxiolytic effects to alleviate symptoms of stress, but different types of stressors have varying effects on alcohol intake. Social stress is particularly relevant to alcohol drinking, and a primate model of stress-induced alcohol self-administration would be useful.
Objective
The objective of the study is to determine if social stresses of different lengths and intensities affect voluntary alcohol intake in monkeys.
Materials and methods
Subjects were adult male and female squirrel monkeys (Saimiri sciureus) housed in social colonies. Subjects were trained to drink a solution of ethanol and sucrose, alternated daily with a control solution of quinine and an equal concentration of sucrose in 15-min sessions. Drinking was tested during 20-min acute, social separations and 1-week, extended, social separations. Dominance status was quantified using observational records of social interactions within the colonies. Salivary cortisol was sampled in the home colony and during extended social separation.
Results
Dominance rank was inversely correlated with alcohol intake during social housing but was not correlated with control fluid intake. Acute social separation abolished drinking of both fluids, accompanied by increased anxiety-like behavior. Extended social separation increased salivary cortisol and alcohol drinking but not control fluid intake in males. In females, drinking was unchanged by extended separation.
Conclusions
The chronic stress of social subordination is correlated with increased alcohol drinking. Acute social separation stress suppresses drinking behavior, while extended separation preferentially increases alcohol intake in a subset of individuals. These findings suggest that social stressors of different time-courses and intensities have opposing effects on alcohol self-administration.
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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
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267
Anisman H, Waller TG (1974) Effects of inescapable shock and shock-produced conflict on self selection of alcohol in rats. Pharmacol Biochem Behav 2:27–33
Ator NA, Griffiths RR (1992) Oral self-administration of triazolam, diazepam and ethanol in the baboon: drug reinforcement and benzodiazepine physical dependence. Psychopharmacology (Berl) 108:301–312
Barr CS, Newman TK, Lindell S, Becker ML, Shannon C, Champoux M, Suomi SJ, Higley JD (2004a) Early experience and sex interact to influence limbic–hypothalamic–pituitary–adrenal–axis function after acute alcohol administration in rhesus macaques (Macaca mulatta). Alcohol Clin Exp Res 28:1114–1119
Barr CS, Newman TK, Lindell S, Shannon C, Champoux M, Lesch KP, Suomi SJ, Goldman D, Higley JD (2004b) Interaction between serotonin transporter gene variation and rearing condition in alcohol preference and consumption in female primates. Arch Gen Psychiatry 61:1146–1152
Barrett GM, Shimizu K, Bardi M, Asaba S, Mori A (2002) Endocrine correlates of rank, reproduction, and female-directed aggression in male Japanese macaques (Macaca fuscata). Horm Behav 42:85–96
Blanchard RJ, Hori K, Tom P, Blanchard DC (1987) Social structure and ethanol consumption in the laboratory rat. Pharmacol Biochem Behav 28:437–442
Blanchard DC, Sakai RR, McEwen B, Weiss SM, Blanchard RJ (1993) Subordination stress: Behavioral, brain, and neuroendocrine correlates. Behav Brain Res 58:113–121
Cloninger CR (1987) Neurogenetic adaptive mechanisms in alcoholism. Science 236:410–416
Conger JJ (1956) Alcoholism: theory, problem and challenge. II. Reinforcement theory and the dynamics of alcoholism. Q J Stud Alcohol 17:296–305
Dukelow WR (1978) Reproduction in the squirrel monkeys (Saimiri sciureus). Rec Adv Primatol 2:195–200
Fahlke C, Lorenz JG, Long J, Champoux M, Suomi SJ, Higley JD (2000) Rearing experiences and stress-induced plasma cortisol as early risk factors for excessive alcohol consumption in nonhuman primates. Alcohol Clin Exp Res 24:644–650
Funk D, Harding S, Juzytsch W, Le AD (2005) Effects of unconditioned and conditioned social defeat on alcohol self-administration and reinstatement of alcohol seeking in rats. Psychopharmacology (Berl) 183:341–349
Grant KA, Waters CA, Green-Jordan K, Azarov A, Szeliga KT (2000) Characterization of the discriminative stimulus effects of GABA(A) receptor ligands in macaca fascicularis monkeys under different ethanol training conditions. Psychopharmacology (Berl) 152:181–188
Higley JD, Hasert MF, Suomi SJ, Linnoila M (1991) Nonhuman primate model of alcohol abuse: effects of early experience, personality, and stress on alcohol consumption. Proc Natl Acad Sci USA 88:7261–7265
Higley JD, Suomi SJ, Linnoila M (1992) A longitudinal assessment of CSF monoamine metabolite and plasma cortisol concentrations in young rhesus monkeys. Biol Psychiatry 32:127–145
Higley JD, Suomi SJ, Linnoila M (1996a) A nonhuman primate model of type II excessive alcohol consumption? Part 1. Low cerebrospinal fluid 5-hydroxyindoleacetic acid concentrations and diminished social competence correlate with excessive alcohol consumption. Alcohol Clin Exp Res 20:629–642
Higley JD, Suomi SJ, Linnoila M (1996b) A nonhuman primate model of type II alcoholism? Part 2. Diminished social competence and excessive aggression correlates with low cerebrospinal fluid 5-hydroxyindoleacetic acid concentrations. Alcohol Clin Exp Res 20:643–650
Hopf S, Hartmann-Wiesner E, Kuhlmorgen B, Mayer S (1974) The behavioral repertoire of the squirrel monkey (saimiri). Folia Primatol (Basel) 21:225–249
Klosterman LL, Murai JT, Siiteri PK (1986) Cortisol levels, binding, and properties of corticosteroid-binding globulin in the serum of primates. Endocrinology 118:424–434
Kornet M, Goosen C, Ribbens LG, van Ree JM (1990) Analysis of spontaneous alcohol drinking in rhesus monkeys. Physiol Behav 47:679–684
Kraemer GW, McKinney WT (1985) Social separation increases alcohol consumption in rhesus monkeys. Psychopharmacology (Berl) 86:182–189
Lynch WJ, Kushner MG, Rawleigh JM, Fiszdon J, Carroll ME (1999) The effects of restraint stress on voluntary ethanol consumption in rats. Exp Clin Psychopharmacol 7:318–323
Lyons DM, Wang OJ, Lindley SE, Levine S, Kalin NH, Schatzberg AF (1999) Separation induced changes in squirrel monkey hypothalamic–pituitary–adrenal physiology resemble aspects of hypercortisolism in humans. Psychoneuroendocrinology 24:131–142
Mandillo S, Titchen K, Miczek KA (1998) Ethanol drinking in socially housed squirrel monkeys. Behav Pharmacol 9:363–367
Miczek KA, Yoshimura H (1982) Disruption of primate social behavior by d-amphetamine and cocaine: Differential antagonism by antipsychotics. Psychopharmacology (Berl) 76:163–171
Pacak K, Palkovits M (2001) Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. Endocr Rev 22:502–548
Pohorecky LA (1990) Interaction of ethanol and stress: research with experimental animals—an update. Alcohol Alcohol 25:263–276
Pohorecky LA (1991) Stress and alcohol interaction: an update of human research. Alcohol Clin Exp Res 15:438–459
Sapolsky RM, Alberts SC, Altmann J (1997) Hypercortisolism associated with social subordinance or social isolation among wild baboons. Arch Gen Psychiatry 54:1137–1143
Shively CA (1998) Social subordination stress, behavior, and central monoaminergic function in female cynomolgus monkeys. Biol Psychiatry 44:882–891
Shively CA, Laber-Laird K, Anton RF (1997) Behavior and physiology of social stress and depression in female cynomolgus monkeys. Biol Psychiatry 41:871–882
Spanagel R, Montkowski A, Allingham K, Stohr T, Shoaib M, Holsboer F, Landgraf R (1995) Anxiety: a potential predictor of vulnerability to the initiation of ethanol self-administration in rats. Psychopharmacology (Berl) 122:369–373
Stewart RB, Bass AA, Wang NS, Meisch RA (1996) Ethanol as an oral reinforcer in normal weight rhesus monkeys: dose–response functions. Alcohol 13:341–346
Swendsen JD, Tennen H, Carney MA, Affleck G, Willard A, Hromi A (2000) Mood and alcohol consumption: an experience sampling test of the self-medication hypothesis. J Abnorm Psychol 109:198–204
Tiefenbacher S, Lee B, Meyer JS, Spealman RD (2003) Noninvasive technique for the repeated sampling of salivary free cortisol in awake, unrestrained squirrel monkeys. Am J Primatol 60:69–75
van Erp AM, Miczek KA (2001) Persistent suppression of ethanol self-administration by brief social stress in rats and increased startle response as index of withdrawal. Physiol Behav 73:301–311
van Erp AM, Tachi N, Miczek KA (2001) Short or continuous social stress: suppression of continuously available ethanol intake in subordinate rats. Behav Pharmacol 12:335–342
Vivian JA, Green HL, Young JE, Majerksy LS, Thomas BW, Shively CA, Tobin JR, Nader MA, Grant KA (2001) Induction and maintenance of ethanol self-administration in cynomolgus monkeys (Macaca fascicularis): long-term characterization of sex and individual differences. Alcohol Clin Exp Res 25:1087–1097
Weerts EM, Miczek KA (1996) Primate vocalizations during social separation and aggression: effects of alcohol and benzodiazepines. Psychopharmacology (Berl) 127:255–264
Willinger U, Lenzinger E, Hornik K, Fischer G, Schonbeck G, Aschauer HN, Meszaros K, European fluvoxamine in alcoholism study group (2002) Anxiety as a predictor of relapse in detoxified alcohol-dependent patients. Alcohol 37:609–612
Winslow JT, Miczek KA (1985) Social status as determinant of alcohol effects on aggressive behavior in squirrel monkeys (Saimiri sciureus). Psychopharmacology (Berl) 85:167–172
Winslow JT, Miczek KA (1988) Androgen dependency of alcohol effects on aggressive behavior: a seasonal rhythm in high-ranking squirrel monkeys. Psychopharmacology (Berl) 95:92–98
Wolffgramm J, Heyne A (1991) Social behavior, dominance, and social deprivation of rats determine drug choice. Pharmacol Biochem Behav 38:389–399
Zumpe D, Michael RP (1986) Dominance index: a simple measure of relative dominance status in primates. Am J Primatol 10:291–300
Acknowledgment
This research was supported by USPHS grant (AA013983) from NIAAA (KAM).
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McKenzie-Quirk, S.D., Miczek, K.A. Social rank and social separation as determinants of alcohol drinking in squirrel monkeys. Psychopharmacology 201, 137–145 (2008). https://doi.org/10.1007/s00213-008-1256-y
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DOI: https://doi.org/10.1007/s00213-008-1256-y