Role of the limbic system in dependence on drugs

Annals of Medicine

Volumn 30, Issue 4, 1998, Pages 397-405

  Rodríguez De Fonseca, Fernando ^a   Navarro, Miguel ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Accumbens; Addiction; Amygdala; Autonomic nervous system; Corticotrophin releasing factor; Dependence; Drugs; Glucocorticoids; Limbic system; Reinforcement; Withdrawal

Indexed keywords

GLUCOCORTICOID;

ADRENAL GLAND; AMYGDALOID NUCLEUS; BEHAVIOR; DRUG ABUSE; DRUG DEPENDENCE; DRUG EXPOSURE; DRUG WITHDRAWAL; DYSPHORIA; EMOTION; FEEDBACK SYSTEM; HUMAN; LIMBIC SYSTEM; MOTIVATION; PRIORITY JOURNAL; REVIEW; STRESS; WITHDRAWAL SYNDROME;

EID: 0031696989     PISSN: 07853890     EISSN: None     Source Type: Journal    
DOI: 10.3109/07853899809029940     Document Type: Review

References (88)

1. Broca P. Anatomie comparée de circonvolutions cérébrales. Le grand lobe limbique et la scissure limbique dans la série des mammifères. Rev Anthropol 1878; 1: 385-498.
2. Papez JW. A proposed mechanism of emotion. Arch Neurol Psychiatry 1937; 38: 725-43.
3. MacLean PD. The limbic system ("visceral brain") and emotional behavior. Arch Neurol Psychiatry 1955; 73: 130-4.
4. Niemvenhuys R, Voogd J, van Huijzen Chr. The Human Central Nervous System. A Synopsis and Atlas. 3rd edn. Berlin: Springer-Verlag; 1988.
5. Isaacson RL. The Limbic System. 2nd edn. New York: Plenum Press; 1982.
6. Kandel ER, Schwartz JH, Jessell TM. Principles of Neural Science. 3rd edn. New York: Prentice Hall; 1991.
7. Reul JMHM, De Kloet ER. Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 1985; 117: 2505-11.
8. Harfstrand A, Fuxe K, Cintra A, et al. Glucocorticoid receptor immunoreactivity in monoaminergic neurons in rat brain. Proc Natl Acad Sci U S A 1986; 83: 9779-83.
9. Olds J, Milner P. Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain. J Comp Physiol Psychol 1954; 47: 419-27.
10. Valenstein ES. The anatomical locus of reinforcement. Prog Physiol Psychol 1966; 1: 149-90.
11. Killam KF, Olds J, Sinclair J. Further studies on the effects of centrally acting drugs on self-stimulation. J Pharmacol Exp Ther 1957; 119: 157.
12. Gardner EL. Brain reward mechanisms. In: Lowinson JH, Ruiz P, Millman RB, Langrod JG, eds. Substance Abuse: A Comprehensive Textbook. 3rd edn. Baltimore: Williams and Wilkins; 1997: 51-85.
13. Bozarth MA, Wise RA. Intracranial self-administration of morphine into the ventral tegmental area of rats. Life Sci 1981; 28: 551-5.
14. Goeders NE, Smith JE. Cortical involvement in cocaine reinforcement. Science 1983; 221: 773-5.
15. Crow T. A map of the rat mesencephalon for electrical self-stimulation. Brain Res 1972; 185: 265-73.
16. Koob GF, Robledo P, Markou A, Caine SB. The mesocortico-limbic circuit in drug dependence and reward - a role for extended amygdala? In: Kalivas PW, Barnes CD, eds. Limbic Motor Circuits and Neuropsychiatry. Boca Raton, FL: CRC Press; 1993: 289-309.
17. Gysling K, Wang RY. Morphine-induced activation of A10 dopamine neurons in rat brain. Brain Res 1983; 277: 119-27.
18. Pontieri FE, Tanda G, Di Chiara G. Intravenous cocaine, morphine and amphetamine preferentially increase extracellular dopamine in the "shell" as compared with the "core" of the rat nucleus accumbens. Proc Natl Acad Sci U S A 1995; 92: 12304-8.
19. Imperato A, Mulas A, Di Chiara G. Nicotine preferentially stimulates dopamine release in the limbic system of freely moving rats. Eur J Pharmacol 1986; 132: 337-8.
20. Imperato A, Di Chiara G. Preferential stimulation of dopamine release in the nucleus accumbens of freely moving rats by ethanol. J Pharmacol Exp Ther 1986; 239: 219-28.
21. 9-tetrahydrocannabinol produces naloxone-blockable enhancement of presynaptic basal dopamine efflux in nucleus accumbens of conscious, freely-moving rats as measured by intracerebral microdialysis. Psychopharmacology 1990; 102: 156-62.
22. Bals-Kubik R, Ableitner A, Herz A, Shippenberg T. Neuroanatomical sites mediating the motivational effects of opioids as mapped by the conditioned place preference paradigm in rats. J Pharmacol Exp Ther 1993; 264: 489-95.
23. Koob GF, Nestler EJ. The neurobiology of drug addiction. J Neuropsychiatry Clin Neurosci 1997; 9: 482-97.
24. Robinson TE, Berridge KC. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev 1993; 18: 247-91.
25. Rodríguez de Fonseca F, Rubio P, Martín-Calderón JL, Caine SB, Koob GF, Navarro M. The dopamine receptor agonist 7-OH-DPAT modulates the acquisition and expression of morphine-induced place preference. Eur J Pharmacol 1995; 274: 47-55.
26. Brown EB, Robertson GS, Fibiger HC. Evidence for conditional neuronal activation following exposure to a cocaine-paired environment: role for forebrain limbic structures. J Neurosci 1992; 12: 4112-21.
27. Schultz W, Dayan P, Montague PR. A neural substrate for prediction and reward. Science 1997; 275: 1593-9.
28. Caine SB, Koob GF. Modulation of cocaine self-administration in the rat through D-3 dopamine receptors. Science 1993; 260: 1814-6.
29. Epping-Jordan MP, Markou A, Koob GF. The dopamine D-1 receptor antagonist SCH 23390 injected into the dorsolateral bed nucleus of stria terminalis decreased cocaine reinforcement in the rat. Brain Res 1998; 784: 105-15.
30. Everitt BJ, Morris KA, O'Brien A, Robbins TW. The basolateral amygdala-ventral striatal system and conditioned place preference: further evidence of limbic-striatal interactions underlying reward-related processes. Neuroscience 1991; 42: 1-18.
31. Breiter HC, Gollub RL, Weisskoff RM, et al. Acute effects of cocaine on human brain activity and emotion. Neuron 1997; 19: 591-611.
32. Ketter T, Andreason P George M, et al. Anterior paralimbic mediation of procaine-induced emotional and psychosensory experiences. Arch Gen Psychiatry 1996; 53: 59-69.
33. Craig AD, Reiman EM, Evans A, Bushnell MC. Functional imaging of an illusion of pain. Nature 1996; 384: 259-60.
34. LeDoux JE. Emotional memory: in search of systems and synapses. Ann N Y Acad Sci 1993; 702: 149-57.
35. Morgan MA, Romanski LM, LeDoux JE. Extinction of emotional learning: contribution of medial prefrontal cortex. Neurosci Lett 1993; 163: 109-13.
36. Lisoprawski A, Herve D, Blanc G, Glowinski J, Tassin JP. Selective activation of the mesocortico-frontal dopaminergic neurons by lesion of the habenula in the rat. Brain Res 1980; 183: 229-34.
37. Wolffgramm J, Heyne A. From controlled drug intake to loss of control: the irreversible development of drug addiction in the rat. Behav Brain Res 1995; 70: 77-94.
38. Koob GF, Carrera MRA, Gold LH, et al. Substance dependence as a compulsive behavior. J Psychopharmacol 1998; 12: 39-48
39. World Health Organization. International Statistical Classification of Diseases and Related Health Problems. 10th revision. Geneva: World Health Organization; 1990.
40. Schulteis G, Koob GF. Reinforcement processes in opiate addiction: a homeostatic model. Neurochem Res 1996; 21: 1437-54.
41. Koob GF, LeMoal, M. Drug abuse: hedonic homeostatic dysregulation. Science 1997: 278, 52-8.
42. Grasing K, Wang A, Schlussman S. Behavioral measures of anxiety during opiate withdrawal. Behav Brain Res 1996; 80:195-201.
43. Knapp DJ, Duncan GE, Crews FT, Breese GR. Induction of Fos-like proteins and ultrasonic vocalizations during ethanol withdrawal: further evidence for withdrawal-induced anxiety. Alcohol Clin Exp Res 1998; 22: 481-93.
44. Rodríguez de Fonseca F, Carrera MRA, Navarro M, Koob GF, Weiss F. Activation of corticotropin-releasing factor in the limbic system during cannabinoid withdrawal. Science 1997; 276: 2050-4.
45. Schaefer GJ, Michael RP. Changes in response rates and reinforcement thresholds for intracranial self-stimulation during morphine withdrawal. Pharmacol Biochem Behav 1986; 25: 1263-9.
46. Leith NJ, Barret RJ. Amphetamine and the reward system: evidence for tolerance and post-drug depression. Psychopharmacologia 1976; 46: 19-25.
47. Markou A, Koob GF. Postcocaine anhedonia: an animal model of cocaine withdrawal. Neuropsychopharmacology 1991; 4: 17-26.
48. Schulteiss G, Markou A, Cole M, Koob GF. Decreased brain reward produced by ethanol withdrawal. Proc Natl Acad Sci U S A 1995; 92: 5880-4.
49. Epping-Jordan MP, Watkins SS, Koob GF, Markou A. Dramatic decreases in brain reward function during nicotine withdrawal. Nature 1998; 393: 76-9.
50. Weiss F, Markou A, Lorang MT, et al. Basal extracellular dopamine levels in the nucleus accumbens are decreased during cocaine withdrawal after unlimited-access self-administration. Brain Res 1992; 593: 314-8.
51. Weiss F, Parsons LH, Schulteis G, et al. Ethanol self-administration restores withdrawal-associated deficiencies in accumbal dopamine and serotonin release in dependent rats. J Neurosci 1996; 16: 3474-81.
52. Koob GF, Wall TL, Bloom FE. Nucleus accumbens as a substrate for the aversive stimulus effects of opiate withdrawal. Psychopharmacology 1989; 98: 530-4.
53. Parsons LH, Koob GF, Weiss F. Serotonin dysfunction in the nucleus accumbens of rats during withdrawal after unlimited access to intravenous cocaine. J Pharmacol Exp Ther 1995; 274: 1182-91.
54. Harris GC, Aston-Jones G. Involvement of D2 dopamine receptors in the nucleus accumbens in the opiate withdrawal syndrome. Nature 1994; 371: 155-7.
55. Merlo-Pich E, Lorang M, Yeganegh M, et al. Increase of extracellular corticotropin-releasing factor-like immunoreactivity in the amygdala of awake rats during restraint stress and ethanol withdrawal as measured by microdialysis. J Neurosci 1995; 15: 5439-47.
56. Mooler C, Wiklund L, Sommer W, Thorsell A, Heilig M. Decreased experimental anxiety and voluntary ethanol consumption in rats following central but not basolateral amygdala lesions. Brain Res 1997; 760: 94-101.
57. Stinus L, Le Moal M, Koob GF. Nucleus accumbens and amygdala as possible substrates for the aversive stimulus effects of opiate withdrawal. Neuroscience 1990; 37: 767-73.
58. Aggleton JP The contribution of the amygdala to normal and abnormal emotional states. Trends Neurosci 1993; 16: 328-33.
59. Vale W, Spiess J, Rivier C, Rivier J. Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and β-endorphin. Science 1981; 213: 1393-7.
60. Rassnick S, Heinrichs SC, Britton KT, Koob GF. Microinjection of corticotropin-releasing factor into the central nucleus of the amygdala reverses the anxiogenic-like effects of ethanol withdrawal. Brain Res 1993; 605: 25-32
61. Heinrichs SC, Menzaghi F, Schulteis G, Koob GF, Stinus L. Suppression of corticotropin-releasing factor in the amygdala attenuates aversive consequences of morphine withdrawal. Behav Pharmacol 1995; 6: 74-80.
62. Arnold FJL, de Lucas Bueno M, Shiers H, Hanckock DC, Evan GI, Herber J. Expression of c-fos in regions of the basal limbic forebrain following intracerebroventricular corticotropin-releasing factor in unstressed or stressed male rats. Neuroscience 1992; 51: 377-90.
63. Ceccatelli S, Villar M, Goldstein M, Hökfelt T. Expression of c-fos immunoreactivity in transmitter-characterized neurons after stress. Proc Natl Acad Sci U S A 1989; 86: 9569-73.
64. Hayward MD, Duman RS, Nestler EJ. Induction of the c-fos proto-oncogene during opiate withdrawal in the locus coeruleus and other regions of rat brain. Brain Res 1990; 525: 256-66.
65. Cador M, Dumas S, Cole BJ, et al. Behavioral sensitization induced by psychostimulants or stress: search for a molecular basis and evidence for a CRF-dependent phenomenon. Ann N Y Acad Sci 1992; 654: 416-20.
66. Richter RM, Merlo Pich E, Koob GF, Weiss F. Sensitization of cocaine-stimulated increase in extracellular levels of corticotropin-releasing factor from the rat amygdala after repeated administration as determined by intracranial microdialysis. Neurosci Lett 1995; 187: 169-72.
67. Baldwin HA, Koob GF. Rapid induction of conditioned opiate withdrawal. Neuropsychopharmacology 1993; 8: 15-21.
68. Cornish JL, Van den Buuse M. Regional expression of c-fos in rat brain following stimulation of the ventral tegmental area. Neurosci Lett 1996; 220: 17-20.
69. Sloviter RS, Valiquette G, Abrams GM, et al. Selective loss of hippocampal granule cells in the mature rat brain after adrenalectomy. Science 1989; 243: 535-8.
70. Uno H, Tarara R, Else JG, Suleman MA, Sapolsky RM. Hippocampal damage associated with prolonged and fatal stress in primates. J Neurosci 1989; 9: 1705-11.
71. Piazza PV, LeMoal M. Pathophysiological basis of vulnerability to drug abuse: role of an interaction between stress, glucocorticoids and dopaminergic neurons. Annu Rev Pharmacol Toxicol 1996; 36: 359-78.
72. Herman JP, Cullinan WE, Morano MI, Akil H, Watson SJ. Contribution of the ventral subiculum to inhibitory regulation of the hypothalamo-pituitary-adrenal axis. J Neuroendocrinol 1995; 7: 475-82.
73. Bussey TJ, Muir JL, Everitt B, Robbins TW. Dissociable effects on anterior and posterior cingulate cortex on the acquisition of conditional visual discrimination: facilitation of early learning vs. impairment of late learning. Behav Brain Res 1996; 82: 45-6.
74. Thierry AM, Tassin JP, Blanc G, Glowinski J. Selective activation of the mesocortical dopamine system by stress. Nature 1976; 263: 242-3.
75. Robinson TE, Kolb B. Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine. J Neurosci 1997; 17: 8491-7.
76. Geary WA, Wooten GF. Time action profiles of regional cerebral glucose utilization during naloxone-precipitated morphine withdrawal. Brain Res 1986; 399: 181-4.
77. Koob GF, Maldonado R, Stinus L. Neural substrates of opiate withdrawal. Trends Neurosci 1992; 15: 186-91.
78. Punch LJ, Self DW, Nestler EJ, Taylor JR. Opposite modulation of opiate withdrawal behaviors on microinfusion of a protein kinase A inhibitor versus activator into the locus coeruleus or periaqueductal gray. J Neurosci 1997; 17: 8520-7.
79. 37] CRF attenuates the acute actions of the highly potent cannabinoid receptor agonist HU-210 on defensive-withdrawal behavior in rats. J Pharmacol Exp Ther 1996; 276: 56-64.
80. McEwen BS, de Kloet ER, Rostene W. Adrenal steroid receptors and actions in the nervous system. Physiol Rev 1986; 66: 1121-88.
81. Piazza PV, Barrot M, Rougé-Pont F, et al. Supression of glucocorticoid secretion and antipsychotic drugs have similar effects on the mesolimbic dopaminergic transmission. Proc Natl Acad Sci U S A 1996; 93: 15445-50.
82. Piazza PV, Deminiere JM, LeMoal M, Simon H. Factors that predict individual vulnerability to amphetamine self-administration. Science 1989; 245: 1511-3.
83. Goeders NE, Guerin GF. Role of corticosterone in intravenous cocaine self-administration. Neuroendocrinology 1996; 64: 337-48.
84. Roberts AJ, Lessov CN, Phillips TJ. Critical role for glucocorticoid receptors in stress- and ethanol-induced locomotor sensitization. J Pharmacol Exp Ther 1995; 275: 790-7.
85. Shaham Y, Stewart J. Stress reinstates heroin-seeking in drug-free animals: an effect mimicking heroin, not withdrawal. Psychopharmacology 1995; 119: 334-41.
86. Maccari S, Piazza PV, Deminiere JM, et al. Life events-induced decrease of corticosteroid type-1 receptors is associated with reduced corticosterone feedback and enhanced vulnerability to amphetamine self-administration. Brain Res 1991; 547: 7-12.
87. Navarro M, Rodriguez de Fonseca F. Early cannabinoid exposure as a source of vulnerability to opiate addiction: a model in laboratory rodents. Spanish J Psychol 1998; 1: 39-58.
88. Imaki T, Nahan JL, Rivier C, Sawchenko PE, Vale W. Differential regulation of corticotropin-releasing factor mRNA in rat brain regions by glucocorticoids and stress. J Neurosci 1991; 11: 585-99.