Social rank, chronic ethanol self-administration, and diurnal pituitary–adrenal activity in cynomolgus monkeys
- 225 Downloads
Dominance hierarchies affect ethanol self-administration, with greater intake among subordinate animals compared to dominant animals. Excessive ethanol intake disrupts circadian rhythms. Diurnal rhythms of the hypothalamic–pituitary–adrenal axis have not been characterized in the context of ethanol self-administration with regard to social rank.
This study aimed to determine whether diurnal pituitary–adrenal hormonal rhythms account for differences between social ranks in ethanol self-administration or are differentially affected by ethanol self-administration between social ranks.
During alternating individual (n = 11–12) and social (n = 3 groups) housing of male cynomolgus monkeys (Macaca fascicularis), diurnal measures of cortisol and adrenocorticotropic hormone (ACTH) were obtained from plasma samples three times per week. Social rank was determined, ethanol (4 %, w/v) self-administration was induced, and then the monkeys were allowed a choice of water or ethanol for 22 h/day for 49 weeks.
For all social ranks, plasma ACTH was elevated during social housing, but cortisol was stable, although greater among dominant monkeys. Ethanol self-administration blunted the effect of social housing, cortisol, and the diurnal rhythm for both hormones, regardless of daily ethanol intake (1.2–4.2 g/kg/day). Peak ACTH and cortisol were more likely to be observed in the morning during ethanol access. Ethanol, not vehicle, intake was lower during social housing across social ranks. Only dominant monkeys showed significantly lower blood–ethanol concentration during social housing.
There was a low threshold for disruption of diurnal pituitary rhythms by ethanol drinking, but sustained adrenal corticosteroid rhythms. Protection against heavy drinking among dominant monkeys may have constrained ethanol intoxication, possibly to preserve dominance rank.
KeywordsEthanol HPA axis Stress Monkey Cortisol ACTH
This work and preparation of the manuscript was supported by RR000163, AA019431, AA019355, AA10760, AA13541, AA13510, and T32AA007468.
- 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 43:67–82PubMedCrossRefGoogle Scholar
- Barr CS, Dvoskin RL, Yuan Q, Lipsky RH, Gupte M, Hu X, Zhou Z, Schwandt ML, Lindell SG, McKee M, Becker ML, Kling MA, Gold PW, Higley JD, Heilig M, Suomi SJ, Goldman D (2008) CRH haplotype predicts CSF CRH, HPA axis activity, temperament, and alcohol consumption in rhesus macaques. Arch Gen Psychiatry 65:934–944PubMedCrossRefGoogle Scholar
- Bohem C (2004) Hierarchy in the forest: the evolution of egalitarian behavior. Harvard University Press, CambridgeGoogle Scholar
- Boschloo L, Vogelzangs N, Licht CMM, Vreeburg SA, Smit JH, van den Brink W, Veltman DJ, de Geus EJC, Beekman ATF, Penninx BWJH (2011) Heavy alcohol use, rather than alcohol dependence, is associated with dysregulation of the hypothalamic–pituitary–adrenal axis and the autonomic nervous system. Drug Alcohol Depend 116:170–176PubMedCrossRefGoogle Scholar
- Cuzon Carlson VC, Seabold GK, Helms CM, Garg N, Odagiri M, Rau AR, Daunais J, Alvarez VA, Lovinger DM, Grant KA (2011) Synaptic and morphological neuroadaptations in the putamen associated with long-term, relapsing alcohol drinking in primates. Neuropsychopharmacology 36:2513–2528PubMedCrossRefGoogle Scholar
- Dong L, Bilbao A, Laucht M, Henriksson R, Yakovleva T, Ridinger M, Desrivieres S, Clarke T-K, Lourdusamy A, Smolka MN, Cichon S, Blomeyer D, Treutlein J, Perreau-Lenz S, Witt S, Leonardi-Essmann F, Wodarz N, Zill P, Soyka M, Albrecht U, Rietschel M, Lathrop M, Bakalkin G, Spanagel R, Schumann G (2011) Effects of the circadian rhythm gene period 1 (Per1) on psychosocial stress-induced alcohol drinking. Am J Psychiatry 168:1090–1098PubMedCrossRefGoogle Scholar
- Flack JC, De Waal FBM (2004) Dominance style, social power, and conflict management: a conceptual framework. In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: a model for the study of social organization. Cambridge University Press, CambridgeGoogle Scholar
- 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 in nonhuman primates. Alcohol 34:402–418Google Scholar
- Higley JD, Suomi SJ, Linnoila M (1996) A nonhuman primate model of type II excessive alcohol consumption? Part 1. Low cerebrospinal fluid 5-hydroxyindoleaceetic acid concentrations and diminished social competence correlate with excessive alcohol consumption. Alcohol Clin Exp Res 20:629–642Google Scholar
- Kraemer GW, McKinney WT (1985) Social separation increases alcohol consumption in rhesus monkeys. Psychopharmacology 104:367–376Google Scholar
- Lee S, Selvage D, Hansen K, Rivier C (2004) Site of action of acute alcohol administration in stimulating the rat hypothalamic–pituitary–adrenal axis: comparison between the effect of systemic and intracerebroventricular injection of this drug on pituitary and hypothalamic responses. Endocrinology 145:4470–4479PubMedCrossRefGoogle Scholar
- Porcu P, Sogliano C, Ibba C, Piredda M, Tocco S, Marra C, Purdy RH, Biggio G, Concas A (2004) Failure of γ-hydroxybutyric acid both to increase neuroactive steroid concentrations in adrenalectomized–orchiectomized rats and to induce tolerance to its steroidogenic effect in intact animals. Brain Res 1012:160–168PubMedCrossRefGoogle Scholar
- Torres-Farfan C, Valenzuela FJ, Ebensperger R, Méndez N, Campino C, Richter HG, Valenzuela GJ, Serón-Ferré M (2008) Circadian cortisol secretion and circadian adrenal responses to ACTH are maintained in dexamethasone suppressed capuchin monkeys (Cebus paella). Am J Primtol 70:93–100CrossRefGoogle Scholar
- 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 25:1087–1097PubMedCrossRefGoogle Scholar
- Wilhelm I, Born J, Kudielka BM, Schlotz W, Wüst S (2007) Is the cortisol awakening rise a response to awakening? Psychoneuroendocrinology 32:358–366Google Scholar