Skip to main content
Log in

Influence of stressors on the rewarding effects of alcohol in Wistar rats: studies with alcohol deprivation and place conditioning

  • Original Investigation
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

Rationale and objectives

Studies on laboratory animals have provided conflicting results regarding the actions of stressors on the rewarding effects of alcohol. In the present study, we first examined the effects of footshock or social defeat, given during deprivation, on the alcohol deprivation effect (ADE). We then tested the effects of stressors on place conditioning to alcohol, another technique used to measure drug reward.

Methods

Male Wistar rats were trained to drink 10% alcohol in a 24 h access, free-choice design and received intermittent footshock or defeat 5 times during a 2-week alcohol deprivation period, followed by 2 weeks of free access to alcohol. There were three such cycles. In the place conditioning studies, animals received footshock, defeat, or no stress immediately prior to conditioning sessions where they received alcohol (0.6 or 1.0 g/kg, IP) or vehicle injections.

Results

Alcohol intake of footshock-treated animals was significantly higher than that of controls following the first and second, but not the third period of alcohol deprivation and stress exposure. Defeat caused a smaller increase in alcohol intake that was significant only after the first deprivation and stress cycle. In the place conditioning studies, we found that either stressor blocked the place aversion induced by 1.0 g/kg alcohol.

Conclusions

These results demonstrate that stressors can modify the rewarding and aversive properties of alcohol, measured using two different paradigms. Footshock and defeat produced transient, but significant increases in the magnitude of ADE, while exposure to either stressor reduced the aversive effects of a high dose of alcohol measured using the place conditioning paradigm.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Bormann NM, Cunningham CL (1998) Ethanol-induced conditioned place aversion in rats: effect of interstimulus interval. Pharmacol Biochem Behav 59:427–432

    Google Scholar 

  • Bowers WJ, Sabongui AG, Amit Z (1997) The role of ethanol availability on stress-induced increases in ethanol consumption. Alcohol 14:551–556

    Article  CAS  PubMed  Google Scholar 

  • Breese GR, Knapp DJ, Overstreet DH (2003) Stress sensitization of ethanol withdrawal-induced reduction in social interaction: inhibition by CRF-1 and benzodiazepine receptor antagonists and a 5-HT1A receptor agonist. Neuropsychopharmacology 3:1–13

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Buwalda B, Blom WA, Koolhaas JM, van Dijk G (2001) Behavioral and physiological responses to stress are affected by high-fat feeding in male rats. Physiol Behav 73:371–377

    Article  CAS  PubMed  Google Scholar 

  • Cooper ML, Russell M, Skinner JB, Frone MR, Mudar P (1992) Stress and alcohol use: moderating effects of gender, coping and alcohol expectancies. J Abnorm Psychol 101:139–152

    CAS  PubMed  Google Scholar 

  • Franklin SR, Tang AH (1995) Dopamine agonists facilitate footshock-elicited locomotion in rats, and suppress lever-press responding for food. Psychopharmacology 121:480–484

    CAS  PubMed  Google Scholar 

  • Heyser CJ, Schulteis G, Koob GF (1997) Increased ethanol self-administration after a period of imposed ethanol deprivation in rats trained in a limited access paradigm. Alcohol Clin Exp Res 21:784–791

    CAS  PubMed  Google Scholar 

  • Holter SM, Linthorst AC, Reul JM, Spanagel R (2000) Withdrawal symptoms in a long-term model of voluntary alcohol drinking in Wistar rats. Pharmacol Biochem Behav 66:143–151

    PubMed  Google Scholar 

  • Homberg JR, van den Akker M, Raaso HS, Wardeh G, Binnekade R, Schoffelmeer AN, de Vries TJ (2002) Enhanced motivation to self-administer cocaine is predicted by self-grooming behavior and relates to dopamine release in the rat medial prefrontal cortex and amygdala. Eur J Neurosci 15:1542–1550

    Article  PubMed  Google Scholar 

  • Kalivas PW, McFarland K (2003) Brain circuitry and the reinstatement of cocaine-seeking behavior. Psychopharmacology 168:44–56

    Article  CAS  PubMed  Google Scholar 

  • Koob GF (2000) Animal models of craving for ethanol. Addiction 95:S78–S81

    Google Scholar 

  • Koolhaas JM, Meerlo P, de Boer SF, Strubbe JH, Bohus B (1997) The temporal dynamics of the stress response. Neurosci Biobehav Rev 21:775–782

    CAS  PubMed  Google Scholar 

  • Lê AD, Quan B, Juzytsch W, Fletcher PJ, Joharchi N, Shaham Y (1998) Reinstatement of alcohol-seeking by priming injections of alcohol and exposure to stress in rats. Psychopharmacology 135:169–174

    PubMed  Google Scholar 

  • Lê AD, Poulos CX, Harding S, Watchus J, Juzytsch W, Shaham Y (1999) Effects of naltrexone and fluoxetine on alcohol seeking induced by priming injections of alcohol and exposure to stress. Neuropsychopharmacology 21:435–444

    Google Scholar 

  • Lê AD, Harding S, Juzytsch W, Watchus J, Shalev U, Shaham Y (2000) The role of corticotropin-releasing factor in stress-induced relapse to alcohol-seeking behavior in rats. Psychopharmacology 150:317–324

    Google Scholar 

  • Matsuzawa S, Suzuki S, Misawa M, Nagase H (1998) Involvement of μ- and δ-opioid receptors in the ethanol-associated place preference in rats exposed to foot shock stress. Brain Res 803:169–177

    CAS  PubMed  Google Scholar 

  • Meerlo P, Overkamp GJ, Benning MA, Koolhaas JM, van den Hoofdakker RH (1996a) Long-term changes in open field behaviour following a single social defeat in rats can be reversed by sleep deprivation. Physiol Behav 60:115–119

    CAS  PubMed  Google Scholar 

  • Meerlo P, Overkamp GJ, Daan S, van den Hoofdakker RH, Koolhaas JM (1996b) Changes in behaviour and body weight following a single or double social defeat in rats. Stress 1:21–32

    PubMed  Google Scholar 

  • Mercier S, Canini F, Buguet A, Cespuglio R, Martin S, Bourdon L (2003) Behavioural changes after acute stress: stressor and test type influences. Behav Brain Res 139:167–175

    Article  PubMed  Google Scholar 

  • Rodd ZA, Bell RL, Kuc KA, Murphy JM, Lumeng L, Li T-K, McBride WJ (2003) Effects of repeated alcohol deprivations on operant ethanol self-administration by alcohol-preferring (P) rats. Neuropsychopharmacology 28:1614–1621

    Article  CAS  PubMed  Google Scholar 

  • Rodd-Henricks ZA, McKinzie DL, Murphy JM, McBride WJ, Lumeng L, Li T-K (2000a) The expression of an alcohol deprivation effect in the high-alcohol-drinking replicate rat line is dependent on repeated deprivations. Alcohol Clin Exp Res 24:747–753

    Article  CAS  PubMed  Google Scholar 

  • Rodd-Henricks ZA, McKinzie DL, Shaikh SR, Murphy JM, McBride WJ, Lumeng L, Li T-K (2000b) Alcohol deprivation effect is prolonged in the alcohol preferring (P) rat after repeated deprivations. Alcohol Clin Exp Res 24:8–16

    Article  CAS  PubMed  Google Scholar 

  • Sinclair JD, Senter RJ (1967) Increased preference for ethanol in rats following alcohol deprivation. Psychon Sci 8:11–12

    Google Scholar 

  • Spanagel R (2000) Recent animal models of alcoholism. Alcohol Res Health 24:124–131

    CAS  PubMed  Google Scholar 

  • Spanagel R, Holter SM (2000) Pharmacological validation of a new animal model of alcoholism. J Neural Transm 107:669–680

    CAS  PubMed  Google Scholar 

  • Tornatzky W, Miczek KA (1993) Long-term impairment of autonomic circadian rhythms after brief intermittent social stress. Physiol Behav 53:983–993

    CAS  PubMed  Google Scholar 

  • Tzschentke TM (1998) Measuring reward with the conditioned place preference paradigm: a comprehensive review of drug effects, recent progress and new issues. Prog Neurobiol 56:613–672

    CAS  PubMed  Google Scholar 

  • van der Kooy D, O’Shaughnessy M, Mucha RF, Kalant H (1983) Motivational properties of ethanol in naive rats as studied by place conditioning. Pharmacol Biochem Behav 19:441–445

    PubMed  Google Scholar 

  • van Erp AMM, 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

    PubMed  Google Scholar 

  • van Erp AMM, Tachi N, Miczek KA (2001) Short or continuous social stress: suppression of continuously available ethanol intake in subordinate rats. Behav Pharmacol 12:335–342

    PubMed  Google Scholar 

  • Vengeliene V, Siegmund S, Singer MV, Sinclair JD, Li T-K, Spanagel R (2003) A comparative study on alcohol-preferring rat lines: effects of deprivation and stress phases on voluntary alcohol intake. Alcohol Clin Exp Res 27:1048–1054

    PubMed  Google Scholar 

  • Weinstock M, Poltyrev T, Schorer-Apelbaum D, Men D, McCarty R (1998) Effect of prenatal stress on plasma corticosterone and catecholamines in response to footshock in rats. Physiol Behav 64:439–444

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from the NIAAA to Dr. A.D. Lê. The authors wish to thank Zhaoxia Li and Stephen Harding for their valuable technical assistance during the running of this experiment.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. Funk.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Funk, D., Vohra, S. & Lê, A.D. Influence of stressors on the rewarding effects of alcohol in Wistar rats: studies with alcohol deprivation and place conditioning. Psychopharmacology 176, 82–87 (2004). https://doi.org/10.1007/s00213-004-1859-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-004-1859-x

Keywords

Navigation