Psychopharmacology

, Volume 168, Issue 1–2, pp 170–176

The role of corticosterone in food deprivation-induced reinstatement of cocaine seeking in the rat

  • Uri Shalev
  • Michela Marinelli
  • Michael H. Baumann
  • Pier-Vincenzo Piazza
  • Yavin Shaham
Original Investigation

Abstract

Rational and objectives.

Acute 1-day food deprivation stress reinstates heroin seeking in rats, but the generality of this effect to other drugs, and its underlying mechanisms, are largely unknown. Here we studied whether food deprivation would reinstate cocaine seeking and whether the stress hormone, corticosterone, is involved in this effect.

Methods.

Rats were trained to press a lever for cocaine for 10–12 days (0.5–1.0 mg/kg per infusion, IV, 4 h/day) and were then divided into four groups that underwent different manipulations of plasma corticosterone levels: (1) bilateral adrenalectomy (ADX) surgery, (2) ADX surgery+50-mg corticosterone pellets (ADX+P), (3) ADX surgery+50-mg corticosterone pellets+4-h access (0800–1200 hours) to corticosterone (50 µg/ml) dissolved in a drinking solution (ADX+P/W), or (4) sham surgery. Next, rats were given 7–12 days of extinction training (during which lever presses were not reinforced with cocaine), and after reaching an extinction criterion they were tested for reinstatement of cocaine seeking following exposure to 21 h of food deprivation.

Results.

Food deprivation was found to reinstate cocaine seeking in sham-operated rats, but not in rats in which circulating corticosterone was removed (ADX group). In addition, the effect of food deprivation on reinstatement of cocaine seeking was significantly attenuated in rats maintained on basal diurnal levels of corticosterone (ADX+P group). However, food deprivation reinstated cocaine seeking in rats with limited daily access to additional corticosterone in the drinking water (ADX+P/W group). In this group, corticosterone levels were twice as high as the ADX+P group but were significantly lower than those of sham rats.

Conclusions.

The present data, together with previous work on footshock-induced reinstatement of drug seeking, suggest that corticosterone plays a permissive role in stress-induced reinstatement of cocaine seeking, yet its effects are not associated with the stressor-induced increases in plasma corticosterone levels.

Keywords.

Adrenalectomy Cocaine Corticosterone Extinction Food deprivation Reinstatement Relapse Stress 

References

  1. Abrahamsen GC, Carr KD (1996) Effects of corticosteroid synthesis inhibitors on the sensitization of reward by food restriction. Brain Res 726:39–48Google Scholar
  2. Abrahamsen GC, Berman Y, Carr KD (1995) Curve-shift analysis of self-stimulation in food-restricted rats: relationship between daily meal, plasma corticosterone and reward sensitization. Brain Res 695:186–194Google Scholar
  3. Arriza JL, Weinberger C, Cerelli G, Glaser TM, Handelin BL, Housman DE, Evans RM (1987) Cloning of human mineralocorticoid receptor complementary DNA: structural and functional kinship with the glucocorticoid receptor. Science 237:268–275Google Scholar
  4. Badiani A, Morano MI, Akil H, Robinson TE (1995) Circulating adrenal hormones are not necessary for the development of sensitization to the psychomotor activating effects of amphetamine. Brain Res 673:13–24Google Scholar
  5. Cabeza de Vaca S, Carr KD (1998) Food restriction enhances the central rewarding effect of abused drugs. J Neurosci 18:7502–7510Google Scholar
  6. Cabib S, Orsini C, Le Moal M, Piazza PV (2000) Abolition and reversal of strain differences in behavioral responses to drugs of abuse after a brief experience. Science 289:463–465Google Scholar
  7. Campbell UC, Carroll ME (2001) Effects of ketoconazole on the acquisition of intravenous cocaine self- administration under different feeding conditions in rats. Psychopharmacology 154:311–318Google Scholar
  8. Carr KD (1996) Feeding, drug abuse, and the sensitization of reward by metabolic need. Neurochem Res 21:1455–1467Google Scholar
  9. Carr KD, Simon EJ (1984) Potentiation of reward by hunger is opioid mediated. Brain Res 297:369–373Google Scholar
  10. Carroll ME (1985) The role of food deprivation in the maintenance and reinstatement of cocaine-seeking behavior in rats. Drug Alcohol Depend 16:95–109Google Scholar
  11. Carroll ME, Meisch ME (1984) Increased drug-reinforced behavior due to food deprivation. In: Thompson T, Dews PB, Barrett JE (eds) Advances in behavioral pharmacology. Academic Press, New York, pp 47–88Google Scholar
  12. Carroll ME, Campbell UC, Heideman P (2001) Ketoconazole suppresses food restriction-induced increases in heroin self-administration in rats: sex differences. Exp Clin Psychopharmacol 9:307–316Google Scholar
  13. Dallman MF, Akana SF, Levin N, Walker CD, Bradbury MJ, Suemaru S, Scribner KS (1995) Corticosteroids and the control of function in the hypothalamo-pituitary-adrenal (HPA) axis. Ann N Y Acad Sci 746:22–31Google Scholar
  14. Dallman MF, Akana SF, Bhatnagar S, Bell ME, Choi S, Chu A, Horsley C, Levin N, Meijer O, Soriano LR, Strack AM, Viau V (1999) Starvation: early signals, sensors, and sequelae. Endocrinology 140:4015–4023Google Scholar
  15. De Kloet ER, Reul JM (1987) Feedback action and tonic influence of corticosteroids on brain function: a concept arising from the heterogeneity of brain receptor systems. Psychoneuroendocrinology 12:83–105Google Scholar
  16. De Vries TJ, Schoffelmeer AN, Tjon GH, Nestby P, Mulder AH, Vanderschuren LJ (1996) Mifepristone prevents the expression of long-term behavioural sensitization to amphetamine. Eur J Pharmacol 307:R3–4Google Scholar
  17. Deroche V, Marinelli M, Maccari S, Le Moal M, Simon H, Piazza PV (1995) Stress-induced sensitization and glucocorticoids. I. Sensitization of dopamine-dependent locomotor effects of amphetamine and morphine depends on stress-induced corticosterone secretion. J Neurosci 15:7181–7188Google Scholar
  18. Deroche V, Marinelli M, Le Moal M, Piazza PV (1997) Glucocorticoids and behavioral effects of psychostimulants II: Cocaine intravenous self-administration and reinstatement depend on glucocorticoids levels. J Pharmacol Exp Ther 281:1401–1407Google Scholar
  19. Erb S, Shaham Y, Stewart J (1998) The role of corticotropin-releasing factor and corticosterone in stress- and cocaine-induced relapse to cocaine seeking in rats. J Neurosci 18:5529–5536Google Scholar
  20. Gaiardi M, Bartoletti M, Bacchi A, Gubellini C, Babbini M (1987) Increased sensitivity to the stimulus properties of morphine in food deprived rats. Pharmacol Biochem Behav 26:719–723Google Scholar
  21. Goeders NE (1997) A neuroendocrine role in cocaine reinforcement. Psychoneuroendocrinology 22:237–259Google Scholar
  22. Goeders NE, Guerin GF (1996) Effects of surgical and pharmacological adrenalectomy on the initiation and maintenance of intravenous cocaine self-administration in rats. Brain Res 722:145–152Google Scholar
  23. Hansen S, Fahlke C, Soderpalm A, Hurd E (1995) Significance of adrenal corticosteroid secretion for the food-induced enhancement of alcohol drinking in the rat. Psychopharmacology 121:213–221Google Scholar
  24. Hollenberg SM, Weinberger C, Ong ES, Cerelli G, Oro A, Lebo R, Thompson EB, Rosenfeld MG, Evans RM (1985) Primary structure and expression of a functional human glucocorticoid receptor cDNA. Nature 318:635–641Google Scholar
  25. Kreek MJ, Koob GF (1998) Drug dependence: stress and dysregulation of brain reward systems. Drug Alcohol Depend 51:23–47Google Scholar
  26. Le AD, Harding S, Watchus W, Juzytsch W, Shalev U, Shaham Y (2000) The role of corticotrophin-releasing factor in stress-induced relapse to alcohol-seeking behavior in rats. Psychopharmacology 150:317–324Google Scholar
  27. Le AD, Shaham Y (2002) Relapse to alcohol-taking behavior in rats. Pharmacol Ther 2002:137–156Google Scholar
  28. Mantsch JR, Goeders NE (1999a) Ketoconazole blocks the stress-induced reinstatement of cocaine-seeking behavior in rats: relationship to the discriminative stimulus effects of cocaine. Psychopharmacology 142:399–407Google Scholar
  29. Mantsch JR, Goeders NE (1999b) Ketoconazole does not block cocaine discrimination or the cocaine-induced reinstatement of cocaine-seeking behavior. Pharmacol Biochem Behav 64:65–73Google Scholar
  30. Marinelli M, Piazza PV, Deroche V, Maccari S, Le Moal M, Simon H (1994) Corticosterone circadian secretion differentially facilitates dopamine- mediated psychomotor effect of cocaine and morphine. J Neurosci 14:2724–2731Google Scholar
  31. Marinelli M, Le Moal M, Piazza PV (1996) Acute pharmacological blockade of corticosterone secretion reverses food restriction-induced sensitization of the locomotor response to cocaine. Brain Res 724:251–255Google Scholar
  32. Marinelli M, Rouge-Pont F, Deroche V, Barrot M, De Jesus-Oliveira C, Le Moal M, Piazza PV (1997) Glucocorticoids and behavioral effects of psychostimulants. I: locomotor response to cocaine depends on basal levels of glucocorticoids. J Pharmacol Exp Ther 281:1392–1400Google Scholar
  33. Mason ST (1983) The neurochemistry and pharmacology of extinction behavior. Neurosci Biobehav Rev 7:325–347Google Scholar
  34. Micco DJ Jr, McEwen BS, Shein W (1979) Modulation of behavioral inhibition in appetitive extinction following manipulation of adrenal steroids in rats: implications for involvement of the hippocampus. J Comp Physiol Psychol 93:323–329Google Scholar
  35. Piazza PV, Le Moal M (1996) Pathophysiological basis of vulnerability to drug abuse: interaction between stress, glucocorticoids, and dopaminergic neurons. Annu Rev Pharmacol Toxicol 36:359–378Google Scholar
  36. Piazza PV, Le Moal M (1997) Glucocorticoids as a biological substrate of reward: physiological and pathophysiological implications. Brain Res Rev 25:359–372Google Scholar
  37. Rivet JM, Stinus L, LeMoal M, Mormede P (1989) Behavioral sensitization to amphetamine is dependent on corticosteroid receptor activation. Brain Res 498:149–153Google Scholar
  38. Sarnyai Z (1998) Neurobiology of stress and cocaine addiction. Studies on corticotropin-releasing factor in rats, monkeys, and humans. Ann N Y Acad Sci 851:371–387Google Scholar
  39. Schmidt ED, Tilders FJ, Binnekade R, Schoffelmeer AN, De Vries TJ (1999) Stressor- or drug-induced sensitization of the corticosterone response is not critically involved in the long-term expression of behavioural sensitization to amphetamine. Neuroscience 92:343–352Google Scholar
  40. Schulkin J, Gold PW, McEwen BS (1998) Induction of corticotropin-releasing hormone gene expression by glucocorticoids: implication for understanding the states of fear and anxiety and allostatic load. Psychoneuroendocrinology 23:219–243Google Scholar
  41. Shaham Y, Funk D, Erb S, Brown TJ, Walker CD, Stewart J (1997) Corticotropin-releasing factor, but not corticosterone, is involved in stress-induced relapse to heroin-seeking in rats. J Neurosci 17:2605–2614Google Scholar
  42. Shaham Y, Erb S, Stewart J (2000) Stress-induced relapse to heroin and cocaine seeking in rats: a review. Brain Res Rev 33:13–33Google Scholar
  43. Shalev U, Highfield D, Yap J, Shaham Y (2000) Stress and relapse to drug seeking in rats: studies on the generality of the effect. Psychopharmacology 150:337–346Google Scholar
  44. Shalev U, Yap J, Shaham Y (2001) Leptin attenuates food deprivation-induced relapse to heroin seeking. J Neurosci 21:RC129Google Scholar
  45. Shalev U, Grimm JW, Shaham Y (2002) Neurobiology of relapse to heroin and cocaine: a review. Pharmacol Rev 54:1–42Google Scholar
  46. Sinha R (2001) How does stress increase risk of drug abuse and relapse. Psychopharmacology 158:343–359Google Scholar
  47. Stewart J, de Wit H (1987) Reinstatement of drug-taking behavior as a method of assessing incentive motivational properties of drugs. In: Bozarth MA (ed) Methods of assessing the reinforcing properties of abused drugs. Springer-Verlag, New York, pp 211–227Google Scholar
  48. Thomas BL, Papini MR (2001) Adrenalectomy eliminates the extinction spike in autoshaping with rats. Physiol Behav 72:543–547Google Scholar
  49. Yokel RA (1987) Intravenous self-administration: Response rates, the effects of pharmacological challenges, and drug preference. In: Bozarth MA (ed) Methods of assessing the reinforcing properties of abused drugs. Springer-Verlag, New York, pp 1–34Google Scholar

Copyright information

© Springer-Verlag  2003

Authors and Affiliations

  • Uri Shalev
    • 1
  • Michela Marinelli
    • 2
  • Michael H. Baumann
    • 3
  • Pier-Vincenzo Piazza
    • 2
  • Yavin Shaham
    • 1
  1. 1.Behavioral Neuroscience Branch, IRP/NIDA/NIH, 5500 Nathan Shock Drive, Baltimore, MD 21224, USAUSA
  2. 2.Laboratoire de Psychobiologie des Comportements Adaptatifs, INSERM U.259, Bordeaux, FranceFrance
  3. 3.Medication Discovery Research Branch, IRP/NIDA/NIH, Baltimore, Md., USAUSA

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