Advertisement

Psychobiology

, Volume 19, Issue 1, pp 79–84 | Cite as

Changes in mesolimbic dopamine may explain stress-induced anhedonia

  • Paul Willner
  • Krystyna Golembiowska
  • Violetta Klimek
  • Richard Muscat
Article
  • 221 Downloads

Abstract

The mesolimbic dopamine projection to the limbic forebrain is known to be critically involved in responsiveness to rewards. In two experiments, the consumption of palatable weak sucrose solutions by rats was reduced by chronic exposure to mild unpredictable stress. Increases in the levels of dopamine and serotonin and their metabolites were found in the limbic forebrain of stressed rats; these changes were not present in the caudate nucleus or septal area, or in the brains of meal-fed control animals. In the first experiment (7 weeks of stress), specific binding to dopamine D2 receptors was decreased in limbic forebrain; this change was not seen in the second experiment (3 weeks of stress). We discuss the possible role of these changes in mesolimbic dopamine function in the reduced sensitivity to reward that follows exposure to chronic mild stress.

Keywords

Caudate Nucleus Mild Stress Chronic Mild Stress Inescapable Shock Sucrose Intake 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. American Psychiatric Association (1980). DSM III — Diagnostic and Statistical manual of psychiatric disorders. Washington, DC: Author.Google Scholar
  2. Anderson, D. C., Cole, J., & McVaugh, W.(1968). Variations in unsignalled inescapable preshock as determinants of responses to punishment. Journal of Comparative & Physiological Psychology, 65 (Monograph Suppl.), 1–17.CrossRefGoogle Scholar
  3. Anisman, H. & Zacharko, R. M. (1982). Depression: The predisposing influence of stress. Behavioral & Brain Sciences, 5, 89–137.CrossRefGoogle Scholar
  4. Bailey, C. S., Hsiao, S., & King, J. E. (1986). Hedonic reactivity to sucrose in rats: Modification by pimozide. Physiology & Behavior, 38, 447–452.CrossRefGoogle Scholar
  5. Blanc, G., Herve, D., Simon, H., Lisoprawski, A., Glowinski, J., & Tassin, J. P. (1980). Response to stress of mesocortical frontal dopaminergic neurons in rats after long-term isolation. Nature, 284, 265–276.PubMedCrossRefGoogle Scholar
  6. Blundell, J. E. (1986). Serotonin manipulations and the structure of feeding behaviour. Appetite, 7 (Suppl.), 39–56.PubMedCrossRefGoogle Scholar
  7. Brown, G. W., & Harris, T. (Eds.) (1988). Life events and illness. New York: Guilford Press.Google Scholar
  8. De Cola, J. P., Rosellini, R. A., & Warren, D. A. (1988). A dissociation of the effects of control and prediction. Learning & Motivation, 19, 269–282.CrossRefGoogle Scholar
  9. Dunn, A. J. (1988). Stress-related activation of cerebral dopaminergic systems. Annals of the New York Academy of Sciences, 537, 188–205.PubMedCrossRefGoogle Scholar
  10. Garattini, S., Mennini, T., Bendotti, C, Invernizzi, R., & Samanin, R. (1986). Neurochemical mechanism of action of drugs which modify feeding via the serotonergic system. Appetite, 7 (Suppl.), 15–38.PubMedCrossRefGoogle Scholar
  11. Heffner, T. G., Hartman, J. A., & Seiden, L. S. (1980). Feeding increases dopamine metabolism in the rat brain. Science, 208, 1168–1170.PubMedCrossRefGoogle Scholar
  12. Hernandez, L., & Hoebel, B. G. (1988). Food reward and cocaine increase extracellular dopamine in the nucleus accumbens as measured by microdialysis. Life Sciences, 42, 1705–1712.PubMedCrossRefGoogle Scholar
  13. Hodos, W., & Valenstein, E. S. (1962). An evaluation of response rate as a measure of rewarding intracranial stimulation. Journal of Comparative & Physiological Psychology, 55, 80–84.CrossRefGoogle Scholar
  14. Hoebel, B. G., Hernandez, L., Mclean, S., Stanley, B. G., Aulissi, E. F., Glimcher, P., & Margoun, D. (1981). In B. G. Hoebel & D. Novin (Eds.), The neural basis of feeding and reward (pp. 465-478). Brunswick, ME: Haer Institute.Google Scholar
  15. Kalivas, P. W., & Abhold, R. (1987). Enkephalin release into the ventral tegmental area in response to stress: Modulation of meso corticolimbic dopamine. Brain Research, 414, 339–348.PubMedCrossRefGoogle Scholar
  16. Kanner, A. D., Coyne, J. C, Schaefer, C, & Lazarus, R. S. (1981). Comparison of two modes of stress measurement: Daily hassles and uplifts versus major life events. Journal of Behavioral Medicine, 4, 1–39.PubMedCrossRefGoogle Scholar
  17. Kant, G. J., Eggleston, T., Landman-Roberts, L., Kenion, C. C, Driver, G. C, & Meyerhoff, J. L. (1983). Habituation to repeated stress is stressor specific. Pharmacology, Biochemistry & Behavior, 22, 631–634.CrossRefGoogle Scholar
  18. Katz, R. J. (1982). Animal model of depression: Pharmacological sensitivity of a hedonic deficit. Pharmacology, Biochemistry & Behavior, 16, 965–968.CrossRefGoogle Scholar
  19. Klein, D. F. (1974). Endogenomorphic depression: A conceptual and terminological revision. Archives of General Psychiatry, 31, 447–454.PubMedCrossRefGoogle Scholar
  20. Klimek, V., & Maj, J. (1990). Repeated administration of antidepressant drugs enhanced agonist affinity for mesolimbic D-2 receptors. Journal of Pharmacy & Pharmacology, 41, 555–558.CrossRefGoogle Scholar
  21. Klimek, V., & Nielsen, M. (1987). Chronic treatment with antidepressants decreases the number of [3H]SCH 23390 binding sites in the rat striatum and limbic system. European Journal of Pharmacology, 139, 163–169.PubMedCrossRefGoogle Scholar
  22. Lloyd, C. (1980a). Life events and depressive disorders reviewed: 1. Events as predisposing factors. Archives of General Psychiatry, 37, 529–535.PubMedCrossRefGoogle Scholar
  23. Lloyd, C. (1980b). Life events and depressive disorders reviewed: 2. Events as precipitating factors. Archives of General Psychiatry, 37, 541–548.PubMedCrossRefGoogle Scholar
  24. Miliaressis, E., & Malette, J. (1987). Summation and saturation properties in the rewarding effect of brain stimulation. Physiology & Behavior, 41, 595–604.CrossRefGoogle Scholar
  25. Muscat, R., Sampson, D., PHILLIPS, G., & Willner, P. (1989). Animal model of depression: Indirect evidence of dopamine dysfunction. Behavioural Pharmacology, 1 (Suppl. 1), 55.Google Scholar
  26. Muscat, R., Sampson, D., & Willner, P. (1990). Dopaminergic mechanism of imipramine action in an animal model of depression. Biological Psychiatry, 28, 223–230.PubMedCrossRefGoogle Scholar
  27. Muscat, R., Towell, A., & Willner, P. (1988). Changes in dopamine autoreceptor sensitivity in an animal model of depression. Psycho-pharmacology, 94, 545–550.CrossRefGoogle Scholar
  28. Muscat, R., & Willner, P. (1989). Effects of selective dopamine receptor antagonists on sucrose consumption and preference. Psycho-pharmacology, 99, 98–102.CrossRefGoogle Scholar
  29. Nelson, J. C, & Charney, D. S. (1981). The symptoms of major depression. American Journal of Psychiatry, 138, 1–13.PubMedCrossRefGoogle Scholar
  30. Phillips, A. G., Blaha, C. D., & Fibiger, H. C. (1989). Neurochemical correlates of brain-stimulation reward measured by ex vivo and in vivo analyses. Neuroscience & Biobehavioral Reviews, 13, 99–104.CrossRefGoogle Scholar
  31. Phillips, G., Muscat, R., & Willner, P. (1989). Dopamine blockade can increase rewarded behaviour: I. Consumption of very sweet solutions. Behavioural Pharmacology, 1 (Suppl. 1), 14.Google Scholar
  32. Rosellini, R. A. (1978). Inescapable shock interferes with the acquisition of an appetitive operant. Animal Learning & Behavior, 6, 155–159.CrossRefGoogle Scholar
  33. Rosellini, R. A., & De COLA, J. P. (1981). Inescapable shock interferes with the acquisition of a low-activity response in an appetitive context. Animal Learning & Behavior, 9, 487–490.CrossRefGoogle Scholar
  34. Rosellini, R. A., De COLA, J. P., PLONSKY, M., WARREN, D. A., & STILLMAN, A. J. (1984). Uncontrollable shock proactively increases sensitivity to response-reinforcer independence in rats. Journal of Experimental Psychology: Animal Behavior Processes, 10, 346–359.PubMedGoogle Scholar
  35. SAMPSON, D., MUSCAT, R., & WILLNER, P. (in press). Reversal of antidepressant action by dopamine antagonists in an animal model of depression. Psychopharmacology.Google Scholar
  36. Stamford, J. A., Muscat, R., O’ Connor, J. J., PATEL, J., Trout, S. J. WIECZOREK, W. J., KRUK, Z. L., & Willner, P. (1991). Voltammetric evidence that subsensitivity to reward following chronic mild stress is associated with increased release ofmesolim-bic dopamine. Manuscript submitted for publication.Google Scholar
  37. Thierry, A. M., Tassin, J. P., Blanc, G., & Glowtnski, J. (1976). Selective activation of the mesocortical dopamine system by stress. Nature, 263, 242–244.PubMedCrossRefGoogle Scholar
  38. Towell, A., Muscat, R., & Willner, P. (1987). Effects of pimozide on sucrose consumption and preference. Psychopharmacology, 92, 262–264.PubMedCrossRefGoogle Scholar
  39. Waraczynski, M., Stellar, J. R., & Gallistel, C. R. (1987). Reward saturation in medial forebrain bundle self-stimulation. Physiology & Behavior, 41, 585–593.CrossRefGoogle Scholar
  40. Willner, P., Muscat, R., Papp, M., & Sampson, D. (1991). Dopamine, depression and antidepressant drugs. In P. Willner & J. Scheel-Kruger (Eds.), The mesolimbic dopamine system: From motivation to action. Chichester, U.K.: Wiley.Google Scholar
  41. Willner, P., Phillips, G., & Muscat, R. (1991). Suppression of rewarded behaviour by neuroleptic drugs: Can’t or won’t, and why? In P. Willner & J. Scheel-Kriiger (Eds.), The mesolimbic dopamine system: From motivation to action (pp. 249–270). Chichester, U.K.: Wiley.Google Scholar
  42. WILLNER, P., SAMPSON, D., PAPP, M., PHILLIPS, G., & MUSCAT, R. (in press). Animal models of anhedonia. In P. Simon, P. Soubrie, & D. Widlocher (Eds.), Animal models of psychiatric disorders (Vol. 3). Basel: Karger.Google Scholar
  43. Willner, P., Towell, A., Sampson, D., Sophokleous, S., & Muscat, R. (1987). Reduction of sucrose preference by chronic mild stress and its restoration by a tricyclic antidepressant. Psychopharmacology, 93, 358–364.PubMedCrossRefGoogle Scholar
  44. Wise, R. A. (1982). Neuroleptics and operant behavior: The anhedonia hypothesis. Behavioral & Brain Sciences, 5, 39–87.CrossRefGoogle Scholar
  45. Wise, R. A., & Bozarth, M. A. (1984). Brain reward circuitry: Four elements “wired” in apparent series. Brain Research Bulletin, 12, 203–208.PubMedCrossRefGoogle Scholar
  46. Zacharko, R. M., & Anisman, H. (1991). Stressor-provoked alterations of intracranial self-stimulation in the mesocorticolimbic dopamine system: An animal model of depression. In P. Willner & J. Scheel-Kriiger (Eds.), The mesolimbic dopamine system: From motivation to action (pp. 409–440). Chichester, U.K.: Wiley.Google Scholar
  47. Zacharko, R. M., Bowers, W. J., & Anisman, H. (1984). Responding for brain stimulation: Stress and desmethylimipramine. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 8, 601–606.CrossRefGoogle Scholar
  48. Zacharko, R. M., Bowers, W. J., Kokkinidis, L., & Anisman, H. (1983). Region specific reductions of intracranial self-stimulation after uncontrollable stress: Possible effects on reward processes. Behavioral Brain Research, 9, 129–141.CrossRefGoogle Scholar

Copyright information

© Psychonomic Society, Inc. 1991

Authors and Affiliations

  • Paul Willner
    • 1
  • Krystyna Golembiowska
    • 2
  • Violetta Klimek
    • 2
  • Richard Muscat
    • 1
  1. 1.Department of PsychologyCity of London PolytechnicLondonEngland
  2. 2.Polish Academy of SciencesKrakowPoland

Personalised recommendations