Stress, depression and the mesolimbic dopamine system

Abstract The present review was aimed at re-evaluating results obtained from animal models of depression based on experimental stressors in the light of the most recent data on the effects of stress on mesolimbic dopamine (DA) functioning. The data reviewed reveal that the effects of stressful experiences on behaviour and on mesoaccumbens DA functioning can be very different or even opposite depending on the behavioural controllability of the situation, the genetic background of the organism and its life history. Exposure to a single unavoidable/uncontrollable aversive experience leads to inhibition of DA release in the accumbens as well as to impaired responding to rewarding and aversive stimuli. Moreover, the data reviewed indicate a strong relationship between these neurochemical and behavioural effects and suggest that they could model stress-induced expression and exacerbation of some depressive symptoms such as anhedonia and feeling of helplessness caused by life events as well as syndromal depression provoked by traumatic experiences in humans. Repeated and chronic stressful experiences can reduce the ability of stressors to disrupt behaviour, induce behavioural sensitisation to psychostimulants and promote adaptive changes of mesolimbic DA functioning. Opposite neural and behavioural changes, however, can be promoted in specific environmental conditions (repeated variable stressful experiences) or in genetically predisposed individuals. Thus, depressive symptoms may not represent the necessary outcome of stress experiences but be promoted by specific environmental conditions and by a genetically determined susceptibility.

[1]  H. Ursin 16 – Activation, Coping, and Psychosomatics , 1978 .

[2]  R. Porsolt,et al.  Behavioural despair in rats: a new model sensitive to antidepressant treatments. , 1978, European journal of pharmacology.

[3]  G. Gessa,et al.  Chronic treatment with antidepressants prevents the inhibitory effect of small doses of apomorphine on dopamine synthesis and motor activity. , 1979, Life sciences.

[4]  K. Roth,et al.  Tail pinch induced stress-arousal facilitates brain stimulation reward , 1979, Physiology & Behavior.

[5]  R. Wise The dopamine synapse and the notion of ‘pleasure centers’ in the brain , 1980, Trends in Neurosciences.

[6]  L. Chiodo,et al.  Repeated tricyclics induce a progressive dopamine autoreceptor subsensitivity independent of daily drug treatment , 1980, Nature.

[7]  B. Carroll,et al.  Acute and chronic stress effects on open field activity in the rat: Implications for a model of depression , 1981, Neuroscience & Biobehavioral Reviews.

[8]  R. Katz,et al.  Animal models and human depressive disorders , 1981, Neuroscience & Biobehavioral Reviews.

[9]  J. Weiss,et al.  Behavioral depression produced by an uncontrollable stressor: Relationship to norepinephrine, dopamine, and serotonin levels in various regions of rat brain , 1981, Brain Research Reviews.

[10]  P. Ropartz,et al.  Effects of isolation, handling and novelty on the pituitary-adrenal response in the mouse , 1982, Psychoneuroendocrinology.

[11]  J. E. Platt,et al.  Chronic restraint stress elicits a positive antidepressant response on the forced swim test. , 1982, European journal of pharmacology.

[12]  R. Katz,et al.  Animal model of depression: Pharmacological sensitivity of a hedonic deficit , 1982, Pharmacology Biochemistry and Behavior.

[13]  S. File,et al.  Cold restraint alters dopamine metabolism in frontal cortex, nucleus accumbens and neostriatum , 1983, Physiology & Behavior.

[14]  S. Maier,et al.  Coping and the stress-induced potentiation of stimulant stereotypy in the rat. , 1983, Science.

[15]  P. Willner Dopamine and depression: A review of recent evidence. I. Empirical studies , 1983, Brain Research Reviews.

[16]  H. Anisman,et al.  Region-specific reductions of intracranial self-stimulation after uncontrollable stress: Possible effects on reward processes , 1983, Behavioural Brain Research.

[17]  J. E. Sherman,et al.  The opioid/nonopioid nature of stress-induced analgesia and learned helplessness. , 1983, Journal of experimental psychology. Animal behavior processes.

[18]  R. Roth,et al.  Footshock and conditioned stress increase 3, 4-dihydroxyphenylacetic acid (DOPAC) in the ventral tegmental area but not substantia nigra , 1985, Brain Research.

[19]  K. Wȩdzony,et al.  Repeated treatment with imipramine or amitriptyline increases the locomotor response of rats to (+)‐amphetamine given into the nucleus accumbens , 1985, The Journal of pharmacy and pharmacology.

[20]  S. Cabib,et al.  A genetic analysis of stereotypy in the mouse: dopaminergic plasticity following chronic stress. , 1985, Behavioral and neural biology.

[21]  M. Le Moal,et al.  Differential reactivity of dopaminergic neurons in the nucleus accumbens in response to different behavioral situations. An in vivo voltammetric study in free moving rats , 1986, Brain Research.

[22]  W. Kostowski,et al.  The effects of antidepressants and electroconvulsive shocks on the functioning of the mesolimbic dopaminergic system: a behavioral study. , 1987, European journal of pharmacology.

[23]  A. Armario,et al.  Chronic stress depresses exploratory activity and behavioral performance in the forced swimming test without altering ACTH response to a novel acute stressor , 1987, Physiology & Behavior.

[24]  N. Swerdlow,et al.  Dopamine, schizophrenia, mania, and depression: Toward a unified hypothesis of cortico-striatopallido-thalamic function , 1987, Behavioral and Brain Sciences.

[25]  B. Scatton,et al.  Tail-pinch stress increases extracellular DOPAC levels (as measured by in vivo voltammetry) in the rat nucleus accumbens but not frontal cortex: antagonism by diazepam and zolpidem , 1987, Brain Research.

[26]  Enhanced functional responsiveness of the dopaminergic system—the mechanism of anti-immobility effects of antidepressants in the behavioural despair test in the rat , 1988, Neuropharmacology.

[27]  F. S. Radhakishun,et al.  Scheduled eating increases dopamine release in the nucleus accumbens of food-deprived rats as assessed with on-line brain dialysis , 1988, Neuroscience Letters.

[28]  S. Cabib,et al.  Effects of immobilization stress on dopamine and its metabolites in different brain areas of the mouse: role of genotype and stress duration , 1988, Brain Research.

[29]  E. Abercrombie,et al.  Differential Effect of Stress on In Vivo Dopamine Release in Striatum, Nucleus Accumbens, and Medial Frontal Cortex , 1989, Journal of neurochemistry.

[30]  H. Anisman,et al.  Pharmacological, Biochemical, and Behavioral Analyses of Depression: Animal Models , 1989 .

[31]  J. Glowinski,et al.  Effect of noxious tail pinch on the discharge rate of mesocortical and mesolimbic dopamine neurons: selective activation of the mesocortical system , 1989, Brain Research.

[32]  Ariel Y. Deutch,et al.  Prefrontal cortical dopamine depletion enhances the responsiveness of mesolimbic dopamine neurons to stress , 1990, Brain Research.

[33]  F. J. White,et al.  A10 somatodendritic dopamine autoreceptor sensitivity following withdrawal from repeated cocaine treatment , 1990, Neuroscience Letters.

[34]  S. Cabib,et al.  Behavioral and biochemical changes monitored in two inbred strains of mice during exploration of an unfamiliar environment , 1990, Physiology & Behavior.

[35]  H. Anisman,et al.  Situation specific effects of stressor controllability on plasma corticosterone changes in mice , 1990, Pharmacology Biochemistry and Behavior.

[36]  P. D’Aquila,et al.  Possible role of dopamine D1 receptor in the behavioural supersensitivity to dopamine agonists induced by chronic treatment with antidepressants , 1990, Brain Research.

[37]  S. Cabib,et al.  Effects of defeat experiences on dopamine metabolism in different brain areas of the mouse , 1990 .

[38]  H. Anisman,et al.  Multiple neurochemical and behavioral consequences of stressors: implications for depression. , 1990, Pharmacology & therapeutics.

[39]  S. Cabib,et al.  Role of genotype in the adaptation of the brain dopamine system to stress , 1990, Neuroscience & Biobehavioral Reviews.

[40]  G. Ossowska,et al.  Chronic stress reduces fighting behavior of rats: The effect of antidepressants , 1991, Pharmacology Biochemistry and Behavior.

[41]  P. Willner Animal models as simulations of depression. , 1991, Trends in pharmacological sciences.

[42]  V. Molina,et al.  Shuttle-box deficits induced by chronic variable stress: Reversal by imipramine administration , 1991, Pharmacology Biochemistry and Behavior.

[43]  M. Le Moal,et al.  Mesocorticolimbic dopaminergic network: functional and regulatory roles. , 1991, Physiological reviews.

[44]  P. Willner,et al.  Changes in mesolimbic dopamine may explain stress-induced anhedonia , 1991, Psychobiology.

[45]  T. Yoshikawa,et al.  Blockade of behavioral sensitization to methamphetamine by lesion of hippocampo-accumbal pathway. , 1991, Life sciences.

[46]  H. Anisman,et al.  Stressor-induced anhedonia in the mesocorticolimbic system , 1991, Neuroscience & Biobehavioral Reviews.

[47]  V. Molina,et al.  Effect of different restraint schedules on the immobility in the forced swim test: Modulation by an opiate mechanism , 1991, Brain Research Bulletin.

[48]  S. Cabib,et al.  Acute stress induces time-dependent responses in dopamine mesolimbic system , 1991, Brain Research.

[49]  S. Cabib,et al.  Genotype-dependent effects of chronic stress on apomorphine-induced alterations of striatal and mesolimbic dopamine metabolism , 1991, Brain Research.

[50]  P. Kalivas,et al.  Effects of cocaine and footshock stress on extracellular dopamine levels in the ventral striatum , 1991, Brain Research.

[51]  A. Imperato,et al.  Changes in brain dopamine and acetylcholine release during and following stress are independent of the pituitary-adrenocortical axis , 1991, Brain Research.

[52]  V. Molina,et al.  Effects of chronic variable stress and antidepressant drugs on behavioral inactivity during an uncontrollable stress: interaction between both treatments. , 1992, Behavioral and neural biology.

[53]  H. Anisman,et al.  Strain-specific alterations in consumption of a palatable diet following repeated stressor exposure , 1992, Pharmacology Biochemistry and Behavior.

[54]  W. Schultz,et al.  Responses of monkey dopamine neurons during learning of behavioral reactions. , 1992, Journal of neurophysiology.

[55]  A. Imperato,et al.  Repeated stressful experiences differently affect limbic dopamine release during and following stress , 1992, Brain Research.

[56]  S. Cabib,et al.  Chronic stress induces strain-dependent sensitization to the behavioral effects of amphetamine in the mouse , 1992, Pharmacology Biochemistry and Behavior.

[57]  S. Cabib,et al.  Nonhuman behavioral models in the genetics of disturbed behavior. , 1992, Journal of psychiatric research.

[58]  W. Haefely,et al.  Antidepressant treatment prevents chronic unpredictable mild stress-induced anhedonia as assessed by ventral tegmentum self-stimulation behavior in rats , 1992, European Neuropsychopharmacology.

[59]  Anthony G. Phillips,et al.  Electrical stimulation of reward sites in the ventral tegmental area increases dopamine transmission in the nucleus accumbens of the rat , 1993, Behavioural Brain Research.

[60]  P Duffy,et al.  Time course of extracellular dopamine and behavioral sensitization to cocaine. I. Dopamine axon terminals , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[61]  T. Robbins,et al.  Enhancement of amphetamine-induced locomotor activity and dopamine release in nucleus accumbens following excitotoxic lesions of the hippocampus , 1993, Behavioural Brain Research.

[62]  T. Robinson,et al.  A microdialysis study of ventral striatal dopamine during sexual behavior in female Syrian hamsters , 1993, Behavioural Brain Research.

[63]  P. Piazza,et al.  Higher and longer stress-induced increase in dopamine concentrations in the nucleus accumbens of animals predisposed to amphetamine self-administration. A microdialysis study , 1993, Brain Research.

[64]  Stefano Puglisi-Allegra,et al.  Repeated stressful experiences differently affect the time-dependent responses of the mesolimbic dopamine system to the stressor , 1993, Brain Research.

[65]  P. Kalivas,et al.  Effects of cocaine and footshock stress on extracellular dopamine levels in the medial prefrontal cortex , 1993, Neuroscience.

[66]  Z. Rossetti,et al.  Depletion of mesolimbic dopamine during behavioral despair: partial reversal by chronic imipramine. , 1993, European journal of pharmacology.

[67]  V. Cestari,et al.  Effects of subchronic minaprine on dopamine release in the ventral striatum and on immobility in the forced swimming test , 1994, Neuroscience Letters.

[68]  S. Cabib,et al.  Opposite responses of mesolimbic dopamine system to controllable and uncontrollable aversive experiences , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[69]  M. Fillenz,et al.  The role ofN-methyl-d-aspartate receptors in the regulation of physiologically released dopamine , 1995, Neuroscience.

[70]  G. Di Chiara The role of dopamine in drug abuse viewed from the perspective of its role in motivation. , 1995, Drug and alcohol dependence.

[71]  G. Chiara The role of dopamine in drug abuse viewed from the perspective of its role in motivation , 1995 .

[72]  M. Marinelli,et al.  Stress-induced sensitization and glucocorticoids. II. Sensitization of the increase in extracellular dopamine induced by cocaine depends on stress-induced corticosterone secretion , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[73]  Michael C. Neale,et al.  Stressful life events, genetic liability, and onset of an episode of major depression in women. , 1995, The American journal of psychiatry.

[74]  J. González-Mora,et al.  Voltammetric and microdialysis monitoring of brain monoamine neurotransmitter release during sociosexual interactions , 1995, Behavioural Brain Research.

[75]  Gaetano Di Chiara,et al.  Erratum: Non-psychostimulant drugs of abuse and anxiogenic drugs activate with differential selectivity dopamine transmission in the nucleus accumbens and in the medial prefrontal cortex of the rat , 1996, Psychopharmacology.

[76]  K. Berridge Food reward: Brain substrates of wanting and liking , 1996, Neuroscience & Biobehavioral Reviews.

[77]  S. Cabib,et al.  Different effects of repeated stressful experiences on mesocortical and mesolimbic dopamine metabolism , 1996, Neuroscience.