Basolateral amygdala lesions impair both cue- and cocaine-induced reinstatement in animals trained on a discriminative stimulus task

Neuroscience

Volumn 121, Issue 3, 2003, Pages 747-757

  Yun, I A ^a   Fields, H L ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN FRANCISCO   (United States)

Author keywords

Analysis of variance; ANOVA; Basolateral amygdala; BLA; Conditioned stimulus; CS; Discriminative stimulus; DS; FR fixed ratio; Motivation; Relapse; Reward; S , non rewarded stimulus, TO, time out; Self administration; Variable interval; VI

Indexed keywords

COCAINE; QUINOLINIC ACID;

ACCURACY; AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; CONDITIONING; CONTROLLED STUDY; DISCRIMINATIVE STIMULUS; INJECTION; MALE; MOTIVATION; NONHUMAN; PREDICTION; PRIORITY JOURNAL; RAT; REWARD; TASK PERFORMANCE;

AMYGDALA; ANIMALS; BEHAVIOR, ANIMAL; COCAINE; COCAINE-RELATED DISORDERS; CONDITIONING, OPERANT; CUES; DISCRIMINATION LEARNING; EXTINCTION, PSYCHOLOGICAL; MALE; QUINOLINIC ACID; RATS; RATS, LONG-EVANS; REINFORCEMENT (PSYCHOLOGY); REINFORCEMENT SCHEDULE; SELF ADMINISTRATION; TIME FACTORS;

EID: 1542538076     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(03)00531-1     Document Type: Article

References (65)

1. Alleweireldt A.T., Weber S.M., Neisewander J.L. Passive exposure to contextual discriminative stimulus reinstates cocaine-seeking behavior in rats. Pharmaco Biochem Behav. 69:2001;555-560.
2. Balleine B.W., Killcross A.S., Dickinson A. The effect of lesions of the basolateral amygdala on instrumental conditioning. J Neurosci. 23:2003;666-675.
3. Baxter M.G., Murray E.A. The amygdala and reward. Nat Rev. 3:2002;563-573.
4. Booze R.M., Lehner A.F., Wallace D.R., Welch M.A., Mactutus C.F. Dose-response cocaine pharmacokinetics and metabolite profile following intravenous administration and arterial sampling in unanesthetized, freely moving male rats. Neurotox Teratol. 19:1997;7-15.
5. Brown E.E., Robertson G.S., Fibiger H.C. Evidence for conditional neuronal activation following exposure to a cocaine-paired environment role of forebrain limbic structures. J Neurosci. 12:1992;4112-4121.
6. Cador M., Robbins T.W., Everitt B.J. Involvement of the amygdala in stimulus-reward associations interaction with the ventral striatum. Neuroscience. 30:1989;77-86.
7. Caine S.B., Lintz R., Koob G.F. Intravenous drug self-administration techniques in animals. Sahgal A. Behavioral neuroscience a practical approach. 1993;117-143 Oxford University Press, New York.
8. Carter B.L., Tiffany S.T. Meta-analysis of cue-reactivity in addiction research. Addiction. 94:1999;327-340.
9. Carter B.L., Tiffany S.T. The cue-availability paradigm the effects of cigarette availability on cue reactivity in smokers. Exp Clin Psychopharmacol. 9:2001;183-190.
10. Childress A.R., Ehrman R.N., McLellan A.T., O'Brien C.P. Classically conditioned responses in opioid and cocaine dependence a role in relapse? NIDA Res Monograph. 84:1988;25-43.
11. Childress A.R., Mozley P.D., McElgin W., Fitzgerald J., Reivich M., O'Brien C.P. Limbic activation during cue-induced cocaine craving. Am J Psychiatry. 156:1999;11-18.
12. Ciccocioppo R., Sanna P.P., Weiss F. Cocaine-predictive stimulus induces drug-seeking behavior and neural activation in limbic brain regions after multiple months of abstinence reversal by D(1) antagonists. Proc Natl Acad Sci USA. 98:2001;1976-1981.
13. Crombag H.S., Shaham Y. Renewal of drug seeking by contextual cues after prolonged extinction in rats. Behav Neurosci. 116:2002;169-173.
14. Davis W.M., Smith S.G. Role of conditioned reinforcers in the initiation, maintenance and extinction of drug-seeking behavior. Pavlov J Biol Sci. 11:1976;222-236.
15. de Wit H., Stewart J. Reinstatement of cocaine-reinforced responding in the rat. Psychopharmacology. 75:1981;134-143.
16. Everitt B.J., Dickenson A., Robbins T.W. The neuropsychological basis of addictive behaviour. Brain Res Rev. 36:2001;129-138.
17. Gracy K.N., Dankiewicz L.A., Weiss F., Koob G.F. Heroin-specific stimuli reinstate operant heroin-seeking behavior in rats after prolonged extinction. Pharmacol Biochem Behav. 65:2000;489-494.
18. Grant S., London E.D., Newlin D.B., Villemagne V.L., Liu X., Contoreggi C., Phillips R.L., Kimes A.S., Margolin A. Activation of memory circuits during cue-elicited cocaine craving. Proc Natl Acad Sci USA. 93:1996;12040-12045.
19. Grimm J.W., See R.E. Dissociation of primary and secondary reward-relevant limbic nuclei in an animal model of relapse. Neuropsychopharmacology. 22:2000;473-479.
20. Hayes R.J., Stanislav R.V., Spector J., Liu X., Gardner E.L. Electrical and chemical stimulation of the basolateral complex of the amygdala reinstates cocaine seeking behavior in the rat. Psychopharmacology. 213:2003;. 1328-1323.
21. Holman J.G., Mackintosh N.J. The control of appetitive instrumental responding does not depend on classical conditioning to the discriminative stimulus. Q J Exp Psychol. 33B:1981;21-31.
22. Howard C.V., Reed M.G. Unbiased stereology three dimensional measurement in microscopy. 1998;Springer, New York.
23. Kantak K.M., Black Y., Valencia E., Green-Jordan K., Eichenbaum H.B. Dissociable effects of lidocaine inactivation of the rostral and caudal basolateral amygdala on the maintenance and reinstatement of cocaine-seeking behavior in rats. J Neurosci. 22:2002;1126-1136.
24. Katner S.N., Magalong J.G., Weiss F. Reinstatement of alcohol-seeking behavior by drug-associated discriminative stimuli after prolonged extinction in the rat. Neuropsychopharmacology. 20:1999;471-479.
25. Kirby K.C., Lamb R.J., Iguchi M.Y., Husband S.D., Platt J.J. Situations occasioning cocaine use and cocaine abstinence strategies. Addiction. 90:1995;1241-1252.
26. Kruse J.M., Overmier J.B., Konz W.A., Rokke E. Pavlovian conditioned stimulus effects upon instrumental choice behavior are reinforcer specific. Learn Motiv. 14:1983;165-181.
27. Kruzich PJ, See RE (2001) Differential contributions of the basolateral and central amygdala in the acquisition and expression of conditioned relapse to cocaine-seeking behavior. J Neurosci 21:RDC155.
28. Lau C.E., Sun L. The pharmacokinetic determinants of the frequency and pattern of intravenous cocaine self-administration in rats by pharmacokinetic modeling. Drug Metabolism and Disposition. 30:2002;254-261.
29. Mackintosh N.J. An analysis of overshadowing and blocking. Q J Exp Psychol. 23:1971;118-125.
30. Malkova L., Gaffan D., Murray E. Excitotoxic lesions of the amygdala fail to produce impairment in visual learning for auditory secondary reinforcement but interferes with reinforcer devaluation effects in rhesus monkeys. J Neurosci. 17:1997;6011-6020.
31. Maren S. Long-term potentiation in the amygdala a mechanism for emotional learning and memory. Trends Neurosci. 22:1999;561-567.
32. Marlatt G.A., Gordon J.R. Relapse prevention. 1985;Guilford Press, New York.
33. McFarland K., Ettenberg A. Reinstatement of drug-seeking behavior produced by heroin-predictive environmental stimuli. Psychopharmacology. 131:1997;86-92.
34. McFarland K., Kalivas P.W. The circuitry mediating cocaine-induced reinstatement of drug-seeking behavior. J Neurosci. 21:2001;8655-8663.
35. McKernan M.G., Shinnick-Gallagher P. Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature. 390:1997;607-611.
36. Meil W.M., See R.E. Lesions of the basolateral amygdala abolish the ability of drug associated cues to reinstate responding during withdrawal from self-administered cocaine. Behav Brain Res. 87:1997;139-148.
37. Meyer R.E., Mirin S.M. The heroin stimulus implications for a theory of addiction. 1979;Plenum Medical Book Company, New York.
38. Muramoto K., Ono T., Nishijo K., Fukuda M. Rat amygdaloid neuron responses during auditory discrimination. Neuroscience. 52:1993;621-636.
39. Neisewander J.L., Baker D.A., Fuchs R.A., Tran-Nguyen L.T., Palmer A., Marshall J.F. Fos protein expression and cocaine-seeking behavior in rats after exposure to a cocaine self-administration environment. J Neurosci. 20:2000;798-805.
40. Nicola S.M., Fields H.L. Ventral tegmental area inactivation reduces the accumbens neuron firing response to motivating stimuli but not reward. Soc Neurosci Abstr. 423:2001;9.
41. Nishijo H., Ono T., Nishino H. Single neuron responses in amygdala of alert monkey during complex sensory stimulation with affective significance. J Neurosci. 8:1988;3570-3583.
42. Panlilio L.V., Weiss S.J., Schindler C.W. Cocaine self-administration increased by compounding discriminative stimuli. Psychopharmacology. 125:1996;202-208.
43. Parkinson J.A., Crofts H.S., McGuigan M., Tomic D.L., Everitt B.J., Roberts A.C. The role of the primate amygdala in conditioned reinforcement. J Neurosci. 21:2001;7770-7780.
44. Paxinos G., Watson C. The rat brain in stereotaxic coordinates. 1997;Academic Press, New York.
45. Pettit H.O., Justice J.B. Dopamine in the nucleus accumbens during cocaine self-administration as studied by in vivo microdialysis. Pharmacol Biochem Behav. 34:1989;899-904.
46. Rescorla R.A. Control of instrumental performance by Pavlovian and instrumental stimuli. J Exp Psychol. 20:1994;44-50.
47. Robins L.N., Helzer J.E., Davis D.H. Narcotic use in southeast Asia and afterward an interview study of 898 Vietnam returnees. Arch Gen Psychiatry. 32:1975;955-961.
48. Robinson T.E., Berridge K.C. The neural bases of drug craving an incentive-sensitization theory of addiction. Brain Res Rev. 18:1993;247-291.
49. Rogan M.T., Staubli U.V., LeDoux J.E. Fear conditioning induces associative long-term potentiation in the amygdala. Nature. 390:1997;604-607.
50. Schoenbaum G., Chiba A.A., Gallagher M. Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning. Nat Neurosci. 1:1998;155-159.
51. Schoenbaum G., Chiba A.A., Gallagher M. Neural encoding in orbitofrontal cortex and basolateral amygdala during olfactory discrimination learning. J Neurosci. 19:1999;1876-1884.
52. Schuster C.R., Woods J.H. The conditioned reinforcing effects of stimuli associated with morphine reinforcement. Int J Addict. 3:1968;223-230.
53. See R.E., Grimm J.W., Kruzich P.J., Rustay N. The importance of a compound stimulus in conditioned drug-seeking behavior following one week of extinction from self-administered cocaine in rats. Drug Alcohol Depend. 57:1999;41-49.
54. Self D.W., Nestler E.J. Relapse to drug-seeking neural and molecular mechanisms. Drug Alcohol Depend. 51:1998;49-60.
55. Shiffman S., Paty J.A., Gnys M., Kassel J.A., Hickcox M. First lapses to smoking within-subjects analysis of real-time reports. J Consult Clin Psychol. 64:1996;366-379.
56. Stewart J., de Wit H., Eikelboom R. Role of unconditioned and conditioned drug effects in the self-administration of opiates and stimulants. Psychol Rev. 91:1984;251-268.
57. Tomie A. Locating reward cue at response manipulandum (CAM) induces symptoms of drug abuse. Neurosci Biobehav Rev. 20:1996;505-535.
58. Tran-Nguyen L.T., Fuchs R.A., Coffey G.P., Baker D.A., O'Dell L.E., Neisewander J.L. Time-dependent changes in cocaine-seeking behavior and extracellular dopamine levels in the amygdala during cocaine withdrawal. Neuropsychopharmacology. 19:1998;48-59.
59. Wasserman E.A., Miller R.R. What's elementary about associative learning? Annu Rev Psychol. 48:1997;573-607.
60. Weisenborn R., Yackey M., Koob G.F., Weiss F. Measures of cocaine-seeking behavior using a multiple schedule of food and drug self-administration in rats. Drug Alcohol Depend. 38:1995;237-246.
61. Weiss F., Maldonado-Vlaar C.S., Parsons L.H., Kerr T.M., Smith D.L., Ben-Shahar O. Control of cocaine-seeking behavior by drug-associated stimuli in rats effects on recovery of extinguished operant-responding and extracellular dopamine levels in amygdala and nucleus accumbens. Proc Natl Acad Sci USA. 97:2000;4321-4326.
62. Weiss R.D., Griffin M.L., Hufford C. Craving in hospitalized cocaine abusers as a predictor of outcome. Am J Drug Alcohol Abuse. 21:1995;289-301.
63. Wertz J.M., Sayette M.A. A review of the effects of perceived drug use opportunity of self-reported urge. Exp Clin Psychopharmacol. 9:2001;3-13.
64. Whitelaw R.B., Markou A., Robbins T.W., Everitt B.J. Excitotoxic lesions of the basolateral amygdala impair the acquisition of cocaine-seeking behavior under a second order schedule of reinforcement. Psychopharmacology. 127:1996;213-224.
65. Wise R.A. Cognitive factors in addiction and nucleus accumbens function some hints from rodent models. Psychobiology. 27:1999;300-310.