Abstract
Rationale
Social environment influences alcohol consumption in humans; however, animal models have only begun to address biological underpinnings of these effects.
Objectives
We investigated whether social influences on alcohol drinking in the prairie vole are specific to the sex of the social partner.
Methods
In Experiment 1, control, sham, and gonadectomized voles were placed either in mesh-divided housing with a same-sex sibling or isolation with access to ethanol. In Experiment 2, animals were given an elevated plus maze test (EPM) and then females were paired with a castrated male followed by isolation or mesh-divided housing with access to ethanol. In Experiment 3, subjects categorized as low or high drinkers based on initial ethanol intake were placed in mesh-divided housing with an opposite-sex partner of the same or opposite drinking group and ethanol access. Subjects were then moved back to isolation for a final ethanol access period.
Results
Same-sex pairs showed social facilitation of drinking similar to previous reports. Gonadectomy did not affect alcohol drinking. Opposite-sex paired animals in Experiment 2 did not differ in alcohol drinking based on social housing. EPM measures suggested a relationship between anxiety-like behaviors and drinking that depended on social environment. Experiment 3 identified moderate changes in alcohol preference based on social housing, but these effects were influenced by the animal’s own drinking behavior and were independent of their partner’s drinking.
Conclusions
Social influences on alcohol self-administration in prairie voles differ based on the sex of a social partner, consistent with human drinking behavior.
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References
Allan CA (1995) Alcohol problems and anxiety disorders—a critical review. Alcohol Alcohol 30:145–151
Almeida SA, Anselmo-Franci JA, Rosa e Silva AA, Carvalho TL (1998) Chronic intermittent immobilization of male rats throughout sexual development: a stress protocol. Exp Physiol 83:701–704
Anacker AM, Ryabinin AE (2010) Biological contribution to social influences on alcohol drinking: evidence from animal models. Int J Environ Res Public Health 7:473–493
Anacker AM, Ahern TH, Young LJ, Ryabinin AE (2011a) Alcohol self-administration inhibits the expression of partner preference in a sex-specific manner in prairie voles. Program No. 469.06. 2011 Neuroscience Meeting Planner. Society for Neuroscience, Washington (Online)
Anacker AMJ, Loftis JM, Kaur S, Ryabinin AE (2011b) Prairie voles as a novel model of socially-facilitated excessive drinking. Addict Biol 16:92–107
Anacker AM, Loftis JM, Ryabinin AE (2011c) Alcohol intake in prairie voles is influenced by the drinking level of a peer. Alcohol Clin Exp Res 35:1884–1890
Bachman JG, Wadsworth KN, O’Mally PM, Johnston LD, Schulenberg JE (1997) Smoking, drinking, and drug use in young adulthood: the impacts of new freedoms and new responsibilities. Lawrence Erlbaum Associates, Inc, Mahwah
Bachman JG, O’Malley PM, Schulenberg JE, Johnston LD, Bryant AL, Merline AC (2002) The decline of substance use in young adulthood: changes in social activities, roles, and beliefs. Lawrence Erlbaum Associates, Inc, Mahwah
Begg DP, Weisinger RS (2008) The role of adrenal or testicular hormones in voluntary ethanol and NaCl intake of crowded and individually housed rats. Physiol Behav 93:408–413
Bosch OJ, Nair HP, Ahern TH, Neumann ID, Young LJ (2009) The CRF system mediates increased passive stress-coping behavior following the loss of a bonded partner in a monogamous rodent. Neuropsychopharmacology 34:1406–1415
Bowler CM, Cushing BS, Carter CS (2002) Social factors regulate female-female aggression and affiliation in prairie voles. Physiol Behav 76:559–566
Bushman BJ, Cooper HM (1990) Effects of alcohol on human aggression: an integrative research review. Psychol Bull 107:341–354
Cailhol S, Mormede P (2001) Sex and strain differences in ethanol drinking: effects of gonadectomy. Alcohol Clin Exp Res 25:594–599
Cavanaugh BL, Lonstein JS (2010) Social novelty increases tyrosine hydroxylase immunoreactivity in the extended olfactory amygdala of female prairie voles. Physiol Behav 100:381–386
Chilcoat HD, Breslau N (1996) Alcohol disorders in young adulthood: effects of transitions into adult roles. J Health Soc Behav 37:339–349
Cho MM, DeVries AC, Williams JR, Carter CS (1999) The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster). Behav Neurosci 113:1071–1079
Colombo G, Agabio R, Lobina C, Reali R, Zocchi A, Fadda F, Gessa GL (1995) Sardinian alcohol-preferring rats: a genetic animal model of anxiety. Physiol Behav 57:1181–1185
Da Silva GE, Ramos A, Takahashi RN (2004) Comparison of voluntary ethanol intake by two pairs of rat lines used as genetic models of anxiety. Braz J Med Biol Res 37:1511–1517
DeVries AC, Carter CS (1999) Sex differences in temporal parameters of partner preference in prairie voles (Microtus ochrogaster). Can J Zool 77:885–889
DeVries AC, DeVries MB, Taymans S, Carter CS (1995) The modulation of pair bonding by corticosterone in female prairie voles (Microtus ochrogaster). Proc Natl Acad Sci USA 92:7744–7748
DeVries AC, Taymans SE, Carter CS (1997) Social modulation of corticosteroid responses in male prairie voles. Ann N Y Acad Sci 807:494–497
Fernandez-Teruel A, Driscoll P, Gil L, Aguilar R, Tobena A, Escorihuela RM (2002) Enduring effects of environmental enrichment on novelty seeking, saccharin and ethanol intake in two rat lines (RHA/Verh and RLA/Verh) differing in incentive-seeking behavior. Pharmacol Biochem Behav 73:225–231
Fisher RA (1921) On the probable error of a coefficient of correlation deduced from a small sample. Metron 1:3–32
Ford MM, Eldridge JC, Samson HH (2002) Ethanol consumption in the female Long-Evans rat: a modulatory role of estradiol. Alcohol 26:103–113
Ford MM, Eldridge JC, Samson HH (2004) Determination of an estradiol dose-response relationship in the modulation of ethanol intake. Alcohol Clin Exp Res 28:20–28
Gotham HJ, Sher KJ, Wood PK (1997) Predicting stability and change in frequency of intoxication from the college years to beyond: individual-difference and role transition variables. J Abnorm Psychol 106:619–629
Henniger MS, Spanagel R, Wigger A, Landgraf R, Holter SM (2002) Alcohol self-administration in two rat lines selectively bred for extremes in anxiety-related behavior. Neuropsychopharmacology 26:729–736
Homish GG, Leonard KE (2008) The social network and alcohol use. J Stud Alcohol Drugs 69:906–914
Hostetler CM, Bales KL (2012) DeltaFosB is increased in the nucleus accumbens by amphetamine but not social housing or isolation in the prairie vole. Neuroscience 210:266–274. doi:10.1016/j.neuroscience.2012.03.019
Hostetler CM, Kowalczyk AS, Griffin LL, Bales KL (2011) CART peptide following social novelty in the prairie vole (Microtus ochrogaster). Brain Res 1414:32–40
Izidio GS, Ramos A (2007) Positive association between ethanol consumption and anxiety-related behaviors in two selected rat lines. Alcohol 41:517–524
Julien RM (2005) A primer of drug action, 10th edn. Worth Publishers, New York
Kalueff AV, Tuohimaa P (2005) The grooming analysis algorithm discriminates between different levels of anxiety in rats: potential utility for neurobehavioural stress research. J Neurosci Methods 143:169–177
Kater RM, Carulli N, Iber FL (1969) Differences in the rate of ethanol metabolism in recently drinking alcoholic and nondrinking subjects. Am J Clin Nutr 22(12):1608–1617
Kushner MG, Abrams K, Borchardt C (2000) The relationship between anxiety disorders and alcohol use disorders: a review of major perspectives and findings. Clin Psychol Rev 20:149–171
Langen B, Fink H (2004) Anxiety as a predictor of alcohol preference in rats? Prog Neuropsychopharmacol Biol Psychiatry 28:961–968
Leonard KE, Eiden RD (2007) Marital and family processes in the context of alcohol use and alcohol disorders. Annu Rev Clin Psychol 3:285–310
Leonard KE, Rothbard JC (1999) Alcohol and the marriage effect. J Stud Alcohol Suppl 13:139–146
Liu Y, Aragona BJ, Young KA, Dietz DM, Kabbaj M, Mazei-Robison M, Nestler EJ, Wang Z (2010) Nucleus accumbens dopamine mediates amphetamine-induced impairment of social bonding in a monogamous rodent species. Proc Natl Acad Sci USA 107:1217–1222
Liu Y, Young KA, Curtis JT, Aragona BJ, Wang Z (2011) Social bonding decreases the rewarding properties of amphetamine through a dopamine D1 receptor-mediated mechanism. J Neurosci 31:7960–7966
McCrady BS, Zucker RA, Molina BS, Ammon L, Ames GM, Longabaugh R (2006) Social environmental influences on the development and resolution of alcohol problems. Alcohol Clin Exp Res 30:688–699
Merline AC, Schulenberg JE, O’Malley PM, Bachman JG, Johnston LD (2008) Substance use in marital dyads: premarital assortment and change over time. J Stud Alcohol Drugs 69:352–361
Miczek KA, Weerts EM, DeBold JF (1993) Alcohol, benzodiazepine-GABAA receptor complex and aggression: ethological analysis of individual differences in rodents and primates. J Stud Alcohol Suppl 11:170–179
Miller-Tutzauer C, Leonard KE, Windle M (1991) Marriage and alcohol use: a longitudinal study of “maturing out”. J Stud Alcohol 52:434–440
Misra PS, Lefévre A, Ishii H, Rubin E, Lieber CS (1971) Increase of ethanol, meprobamate and pentobarbital metabolism after chronic ethanol administration in man and in rats. Am J Med 51(3):346–351
Northcutt KV, Lonstein JS (2009) Social contact elicits immediate-early gene expression in dopaminergic cells of the male prairie vole extended olfactory amygdala. Neuroscience 163:9–22
Pepino MY, Abate P, Spear NE, Molina JC (2002) Disruption of maternal behavior by alcohol intoxication in the lactating rat: a behavioral and metabolic analysis. Alcohol Clin Exp Res 26:1205–1214
Pfaus JG, Pinel JPJ (1989) Alcohol inhibits and disinhibits sexual behavior in the male rat. Psychobiology 17:195–201
Resendez SL, Kuhnmuench M, Krzywosinski T, Aragona BJ (2012) κ-Opioid receptors within the nucleus accumbens shell mediate pair bond maintenance. J Neurosci 32:6771–6784. doi:10.1523/jneurosci.5779-11.2012
Robbins CA (1991) Social roles and alcohol abuse among older men and women. Fam Commun Health 13:37–48
Robinson JA, Sareen J, Cox BJ, Bolton JM (2009) Correlates of self-medication for anxiety disorders: results from the National Epidemiologic Survey on Alcohol and Related Conditions. J Nerv Ment Dis 197:873–878
Russell DW, Booth B, Reed D, Laughlin PR (1997) Personality, social networks, and perceived social support among alcoholics: a structural equation analysis. J Pers 65:649–692
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
Steele CM, Southwick L (1985) Alcohol and social behavior I: the psychology of drunken excess. J Pers Soc Psychol 48:18–34
Stewart RB, Gatto GJ, Lumeng L, Li TK, Murphy JM (1993) Comparison of alcohol-preferring (P) and non-preferring (NP) rats on tests of anxiety and for the anxiolytic effects of ethanol. Alcohol 10:1–10
Tuominen K, Hilakivi LA, Paivarinta P, Korpi ER (1990) Behavior of alcohol-preferring AA and alcohol-avoiding ANA rat lines in tests of anxiety and aggression. Alcohol 7:349–353
Vetter-O’Hagen CS, Spear LP (2011) The effects of gonadectomy on age- and sex-typical patterns of ethanol consumption in Sprague Dawley rats. Alcohol Clin Exp Res 35:2039–2049
Viglinskaya IV, Overstreet DH, Kashevskaya OP, Badishtov BA, Kampov-Polevoy AB, Seredenin SB, Halikas JA (1995) To drink or not to drink: tests of anxiety and immobility in alcohol-preferring and alcohol-nonpreferring rat strains. Physiol Behav 57:937–941
Wilsnack SC, Klassen AD, Shur BE, Wilsnack RW (1991) Predicting onset and chronicity of women’s problem drinking: a five year longitudinal analysis. Amer J Publ Hlth 81:305–318
Winslow JT, Hastings N, Carter CS, Harbaugh CR, Insel TR (1993) A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365:545–548
Young KA, Gobrogge KL, Liu Y, Wang Z (2011a) The neurobiology of pair bonding: insights from a socially monogamous rodent. Front Neuroendocrinol 32:53–69
Young KA, Liu Y, Gobrogge KL, Dietz DM, Wang H, Kabbaj M, Wang Z (2011b) Amphetamine alters behavior and mesocorticolimbic dopamine receptor expression in the monogamous female prairie vole. Brain Res 1367:213–222
Acknowledgments
We gratefully acknowledge Davelle Cocking, Lindsay Swanson, and the Veterinary Medical Unit (VMU) animal care staff from the Portland VA Medical Center for assistance on this project. This research was funded by NIH 5T32AA007468-24 (to CMH) and NIH AA016886 (to AER). This material is the result of work supported with resources and the use of facilities at the Portland VA Medical Center, Portland, Oregon.
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The following research was funded by NIH 5T32AA007468-24 (to CMH) and NIH AA016886 (to AER).
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Hostetler, C.M., Anacker, A.M.J., Loftis, J.M. et al. Social housing and alcohol drinking in male-female pairs of prairie voles (Microtus ochrogaster). Psychopharmacology 224, 121–132 (2012). https://doi.org/10.1007/s00213-012-2836-4
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DOI: https://doi.org/10.1007/s00213-012-2836-4