Parallel and interactive learning processes within the basal ganglia: Relevance for the understanding of addiction

Behavioural Brain Research

Volumn 199, Issue 1, 2009, Pages 89-102

  Belin, David ^a   Jonkman, Sietse ^a   Dickinson, Anthony ^a   Robbins, Trevor W ^a   Everitt, Barry J ^a  

^a University of Cambridge   (United Kingdom)

Author keywords

Addiction; Amygdala; Basal ganglia; Behavioural control; Conditioning; Incentive habits; Learning; Reward; Self administration

Indexed keywords

AMPHETAMINE; CANNABIS; COCAINE; DIAMORPHINE; DOPAMINE; MORPHINE; NICOTINE;

ACTION POTENTIAL; ADDICTION; AMYGDALOID NUCLEUS; AVERSION; BASAL GANGLION; BEHAVIOR CONTROL; BEHAVIOR MODIFICATION; BRAIN DYSFUNCTION; CORPUS STRIATUM; DISEASE COURSE; DRUG ABUSE; DRUG DEPENDENCE; EMOTION; HABIT; HABITUAL ADAPTATION; INSTRUMENTAL CONDITIONING; LEARNING; LIMBIC SYSTEM; MOTIVATION; MOTOR PERFORMANCE; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; NUCLEUS ACCUMBENS; ORBITAL CORTEX; PATHOLOGY; PRIORITY JOURNAL; REINFORCEMENT; RELAPSE; REVIEW; REWARD; SENSORY NERVE; SPINAL GANGLION; STIMULUS RESPONSE; THALAMOCORTICAL TRACT;

ANIMALS; BASAL GANGLIA; BEHAVIOR, ADDICTIVE; CONDITIONING, OPERANT; DOPAMINE; HUMANS; NERVE NET; NUCLEUS ACCUMBENS; REINFORCEMENT (PSYCHOLOGY); SUBSTANCE-RELATED DISORDERS;

EID: 61349196840     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2008.09.027     Document Type: Review

References (212)

1. Koob G.F., and Le Moal M. Neurobiology of addiction (2006), Academic Press, London p. 490
2. Everitt B.J., and Robbins T.W. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 8 11 (2005) 1481-1489
3. Everitt B.J., Dickinson A., and Robbins T.W. The neuropsychological basis of addictive behaviour. Brain Res Brain Res Rev 36 2-3 (2001) 129-138
4. Pierce R.C., and Kalivas P.W. A circuitry model of the expression of behavioral sensitization to amphetamine-like psychostimulants. Brain Res Brain Res Rev 25 2 (1997) 192-216
5. Vanderschuren L.J., De Vries T.J., Wardeh G., Hogenboom F.A., and Schoffelmeer A.N. A single exposure to morphine induces long-lasting behavioural and neurochemical sensitization in rats. Eur J Neurosci 14 9 (2001) 1533-1538
6. Vanderschuren L.J., Schmidt E.D., De Vries T.J., Van Moorsel C.A., Tilders F.J., and Schoffelmeer A.N. A single exposure to amphetamine is sufficient to induce long-term behavioral, neuroendocrine, and neurochemical sensitization in rats. J Neurosci 19 21 (1999) 9579-9586
7. Nicola S.M., Kombian S.B., and Malenka R.C. Psychostimulants depress excitatory synaptic transmission in the nucleus accumbens via presynaptic D1-like dopamine receptors. J Neurosci 16 5 (1996) 1591-1604
8. Ungless M.A., Whistler J.L., Malenka R.C., and Bonci A. Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 411 6837 (2001) 583-587
9. Nestler E.J. Is there a common molecular pathway for addiction?. Nat Neurosci 8 11 (2005) 1445-1449
10. Kolb B., Gorny G., Li Y., Samaha A.N., and Robinson T.E. Amphetamine or cocaine limits the ability of later experience to promote structural plasticity in the neocortex and nucleus accumbens. Proc Natl Acad Sci USA 100 18 (2003) 10523-10528
11. Jedynak J.P., Uslaner J.M., Esteban J.A., and Robinson T.E. Methamphetamine-induced structural plasticity in the dorsal striatum. Eur J Neurosci 25 3 (2007) 847-853
12. Belin D., and Everitt B.J. Cocaine-seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum. Neuron 57 3 (2008) 432-441
13. Takahashi Y., Roesch M.R., Stanlaker T.A., and Schoenbaum G. Cocaine exposure shifts the balance of associative encoding from ventral to dorsolateral striatum. Front Integr Neurosci 1 1 (2007)
14. Alexander G.E., and Crutcher M.D. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13 7 (1990) 266-271
15. Alexander G.E., Crutcher M.D., and DeLong M.R. Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. Prog Brain Res 85 (1990) 119-146
16. Alexander G.E., DeLong M.R., and Strick P.L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9 (1986) 357-381
17. Haber S.N. The primate basal ganglia: parallel and integrative networks. J Chem Neuroanat 26 4 (2003) 317-330
18. Haber S.N., Fudge J.L., and McFarland N.R. Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J Neurosci 20 6 (2000) 2369-2382
19. Mogenson G.J., Jones D.L., and Yim C.Y. From motivation to action: functional interface between the limbic system and the motor system. Prog Neurobiol 14 2-3 (1980) 69-97
20. Cardinal R.N., Parkinson J.A., Hall J., and Everitt B.J. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 26 3 (2002) 321-352
21. Setlow B., Holland P.C., and Gallagher M. Disconnection of the basolateral amygdala complex and nucleus accumbens impairs appetitive pavlovian second-order conditioned responses. Behav Neurosci 116 2 (2002) 267-275
22. Cardinal R.N., Parkinson J.A., Lachenal G., Halkerston K.M., Rudarakanchana N., Hall J., et al. Effects of selective excitotoxic lesions of the nucleus accumbens core, anterior cingulate cortex, and central nucleus of the amygdala on autoshaping performance in rats. Behav Neurosci 116 4 (2002) 553-567
23. Di Ciano P., Cardinal R.N., Cowell R.A., Little S.J., and Everitt B.J. Differential involvement of NMDA, AMPA/kainate, and dopamine receptors in the nucleus accumbens core in the acquisition and performance of pavlovian approach behavior. J Neurosci 21 23 (2001) 9471-9477
24. Hall J., Parkinson J.A., Connor T.M., Dickinson A., and Everitt B.J. Involvement of the central nucleus of the amygdala and nucleus accumbens core in mediating Pavlovian influences on instrumental behaviour. Eur J Neurosci 13 10 (2001) 1984-1992
25. Parkinson J.A., Willoughby P.J., Robbins T.W., and Everitt B.J. Disconnection of the anterior cingulate cortex and nucleus accumbens core impairs Pavlovian approach behavior: further evidence for limbic cortical-ventral striatopallidal systems. Behav Neurosci 114 1 (2000) 42-63
26. Parkinson J.A., Dalley J.W., Cardinal R.N., Bamford A., Fehnert B., Lachenal G., et al. Nucleus accumbens dopamine depletion impairs both acquisition and performance of appetitive Pavlovian approach behaviour: implications for mesoaccumbens dopamine function. Behav Brain Res 137 1-2 (2002) 149-163
27. Parkinson J.A., Olmstead M.C., Burns L.H., Robbins T.W., and Everitt B.J. Dissociation in effects of lesions of the nucleus accumbens core and shell on appetitive pavlovian approach behavior and the potentiation of conditioned reinforcement and locomotor activity by D-amphetamine. J Neurosci 19 6 (1999) 2401-2411
28. Yin H.H., Ostlund S.B., Knowlton B.J., and Balleine B.W. The role of the dorsomedial striatum in instrumental conditioning. Eur J Neurosci 22 2 (2005) 513-523
29. Yin H.H., Knowlton B.J., and Balleine B.W. Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur J Neurosci 19 1 (2004) 181-189
30. Faure A., Haberland U., Conde F., and El Massioui N. Lesion to the nigrostriatal dopamine system disrupts stimulus-response habit formation. J Neurosci 25 11 (2005) 2771-2780
31. Di Chiara G., and Imperato A. Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci USA 85 14 (1988) 5274-5278
32. Volkow N.D., Wang G.J., Telang F., Fowler J.S., Logan J., Childress A.R., et al. Cocaine cues and dopamine in dorsal striatum: mechanism of craving in cocaine addiction. J Neurosci 26 24 (2006) 6583-6588
33. Vanderschuren L.J., Di Ciano P., and Everitt B.J. Involvement of the dorsal striatum in cuecontrolled cocaine seeking. J Neurosci 25 38 (2005) 8665-8670
34. Corbit L.H., Muir J.L., and Balleine B.W. The role of the nucleus accumbens in instrumental conditioning: evidence of a functional dissociation between accumbens core and shell. J Neurosci 21 9 (2001) 3251-3260
35. Corbit L.H., and Balleine B.W. The role of prelimbic cortex in instrumental conditioning. Behav Brain Res 146 1-2 (2003) 145-157
36. Baldwin A.E., Holahan M.R., Sadeghian K., and Kelley A.E. N-methyl-D-aspartate receptor-dependent plasticity within a distributed corticostriatal network mediates appetitive instrumental learning. Behav Neurosci 114 1 (2000) 84-98
37. Smith-Roe S.L., and Kelley A.E. Coincident activation of NMDA and dopamine D1 receptors within the nucleus accumbens core is required for appetitive instrumental learning. J Neurosci 20 20 (2000) 7737-7742
38. Andrzejewski M.E., Spencer R.C., and Kelley A.E. Instrumental learning, but not performance, requires dopamine D1-receptor activation in the amygdala. Neuroscience 135 2 (2005) 335-345
39. McKee B.L., and Kelley A.E. N-methyl-D-aspartate (NMDA) receptor blockade in the anterior cingulate cortex impairs acquisition of instrumental responding for sucrose (2007), Society For Neuroscience Meeting, San Diego
40. Hernandez P.J., Sadeghian K., and Kelley A.E. Early consolidation of instrumental learning requires protein synthesis in the nucleus accumbens. Nat Neurosci 5 12 (2002) 1327-1331
41. Baldwin A.E., Sadeghian K., Holahan M.R., and Kelley A.E. Appetitive instrumental learning is impaired by inhibition of cAMP-dependent protein kinase within the nucleus accumbens. Neurobiol Learn Mem 77 1 (2002) 44-62
42. Weissenborn R., Robbins T.W., and Everitt B.J. Effects of medial prefrontal or anterior cingulate cortex lesions on responding for cocaine under fixed-ratio and second-order schedules of reinforcement in rats. Psychopharmacology (Berl) 134 3 (1997) 242-257
43. Caine S.B., Humby T., Robbins T.W., and Everitt B.J. Behavioral effects of psychomotor stimulants in rats with dorsal or ventral subiculum lesions: locomotion, cocaine self-administration, and prepulse inhibition of startle. Behav Neurosci 115 4 (2001) 880-894
44. Ito R., Robbins T.W., and Everitt B.J. Differential control over cocaine-seeking behavior by nucleus accumbens core and shell. Nat Neurosci 7 4 (2004) 389-397
45. Alderson H.L., Parkinson J.A., Robbins T.W., and Everitt B.J. The effects of excitotoxic lesions of the nucleus accumbens core or shell regions on intravenous heroin self-administration in rats. Psychopharmacology (Berl) 153 4 (2001) 455-463
46. White N.M., and Viaud M. Localized intracaudate dopamine D2 receptor activation during the post-training period improves memory for visual or olfactory conditioned emotional responses in rats. Behav Neural Biol 55 3 (1991) 255-269
47. Carr G.D., and White N.M. Effects of systemic and intracranial amphetamine injections on behavior in the open field: a detailed analysis. Pharmacol Biochem Behav 27 1 (1987) 113-122
48. Carelli R.M. Nucleus accumbens cell firing and rapid dopamine signaling during goal-directed behaviors in rats. Neuropharmacology 47 Suppl. 1 (2004) 180-189
49. Carelli R.M., Ijames S.G., and Crumling A.J. Evidence that separate neural circuits in the nucleus accumbens encode cocaine versus "natural" (water and food) reward. J Neurosci 20 11 (2000) 4255-4266
50. Carelli R.M., and Wondolowski J. Selective encoding of cocaine versus natural rewards by nucleus accumbens neurons is not related to chronic drug exposure. J Neurosci 23 35 (2003) 11214-11223
51. Logan G.D. What is learned during automatization? II. Obligatory encoding of spatial location. J Exp Psychol Hum Percept Perform 24 6 (1998) 1720-1736
52. Dickinson A. Actions and habits: the development of behavioural autonomy. Philos Trans R Soc Lond B Biol Sci 308 1135 (1985) 67-78
53. Balleine B.W., and Dickinson A. Goal-directed instrumental action: contingency and incentive learning and their cortical substrates. Neuropharmacology 37 4-5 (1998) 407-419
54. Dickinson A., Nicholas D.J., and Adams C.D. The effect of the instrumental training contingency on susceptibility to reinforcer devaluation. Q J Exp Psychol 35 B (1983) 35-51
55. Hilário M.R.F., Clouse E., Yin H.H., and Costa R.M. Endocannabinoid signaling is critical for habit formation. Front Integr Neurosci 1 (2007) (Article 6)
56. Mackintosh N.J. The psychology of animal learning (1974), London Academic Press
57. Balleine B., Gerner C., and Dickinson A. Instrumental outcome devaluation is attenuated by the anti-emetic ondansetron. Q J Exp Psychol B 48 3 (1995) 235-251
58. Yin H.H., Knowlton B.J., and Balleine B.W. Inactivation of dorsolateral striatum enhances sensitivity to changes in the action-outcome contingency in instrumental conditioning. Behav Brain Res 166 2 (2006) 189-196
59. Dickinson A., Squire S., Varga Z., and Smith J.W. Omission learning after instrumental pretraining. Q J Exp Psychol 51 B (1998) 271-286
60. Yin H.H., Knowlton B.J., and Balleine B.W. Blockade of NMDA receptors in the dorsomedial striatum prevents action-outcome learning in instrumental conditioning. Eur J Neurosci 22 2 (2005) 505-512
61. Killcross S., and Coutureau E. Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb Cortex 13 4 (2003) 400-408
62. Ostlund S.B., and Balleine B.W. Lesions of medial prefrontal cortex disrupt the acquisition but not the expression of goal-directed learning. J Neurosci 25 34 (2005) 7763-7770
63. Coutureau E., and Killcross S. Inactivation of the infralimbic prefrontal cortex reinstates goal-directed responding in overtrained rats. Behav Brain Res 146 1-2 (2003) 167-174
64. Balleine B.W. Neural bases of food-seeking: affect, arousal and reward in corticostriatolimbic circuits. Physiol Behav 86 5 (2005) 717-730
65. Nelson A., and Killcross S. Amphetamine exposure enhances habit formation. J Neurosci 26 14 (2006) 3805-3812
66. Nordquist R.E., Voorn P., de Mooij-van Malsen J.G., Joosten R.N., Pennartz C.M., and Vanderschuren L.J. Augmented reinforcer value and accelerated habit formation after repeated amphetamine treatment. Eur Neuropsychopharmacol 17 8 (2007) 532-540
67. Dickinson A., Wood N., and Smith J.W. Alcohol seeking by rats: action or habit?. Q J Exp Psychol B 55 4 (2002) 331-348
68. Miles F.J., Everitt B.J., and Dickinson A. Oral cocaine seeking by rats: action or habit?. Behav Neurosci 117 5 (2003) 927-938
69. Canales J.J. Stimulant-induced adaptations in neostriatal matrix and striosome systems: transiting from instrumental responding to habitual behavior in drug addiction. Neurobiol Learn Mem 83 2 (2005) 93-103
70. See R.E., Elliott J.C., and Feltenstein M.W. The role of dorsal vs ventral striatal pathways in cocaine-seeking behavior after prolonged abstinence in rats. Psychopharmacology (Berl) 194 3 (2007) 321-331
71. Fuchs R.A., Branham R.K., and See R.E. Different neural substrates mediate cocaine seeking after abstinence versus extinction training: a critical role for the dorsolateral caudate-putamen. J Neurosci 26 13 (2006) 3584-3588
72. Childress A.R., Mozley P.D., McElgin W., Fitzgerald J., Reivich M., and O'Brien C.P. Limbic activation during cue-induced cocaine craving. Am J Psychiatry 156 1 (1999) 11-18
73. Wong D.F., Kuwabara H., Schretlen D.J., Bonson K.R., Zhou Y., Nandi A., et al. Increased occupancy of dopamine receptors in human striatum during cue-elicited cocaine craving. Neuropsychopharmacology 31 12 (2006) 2716-2727
74. Garavan H., Pankiewicz J., Bloom A., Cho J.K., Sperry L., Ross T.J., et al. Cue-induced cocaine craving: neuroanatomical specificity for drug users and drug stimuli. Am J Psychiatry 157 11 (2000) 1789-1798
75. Ahn S., and Phillips A.G. Dopamine efflux in the nucleus accumbens during within-session extinction, outcome-dependent, and habit-based instrumental responding for food reward. Psychopharmacology (Berl) 191 3 (2007) 641-651
76. Wise R.A. Dopamine, learning and motivation. Nat Rev Neurosci 5 6 (2004) 483-494
77. Tiffany S.T. A cognitive model of drug urges and drug-use behavior: role of automatic and nonautomatic processes. Psychol Rev 97 2 (1990) 147-168
78. Schoenbaum G., and Setlow B. Cocaine makes actions insensitive to outcomes but not extinction: implications for altered orbitofrontal-amygdalar function. Cereb Cortex 15 8 (2005) 1162-1169
79. Pavlov I. Conditioned reflexes (1927), Oxford University Press, Oxford
80. Brown P.L., and Jenkins H.M. Auto-shaping of the pigeon's key-peck. J Exp Anal Behav 11 1 (1968) 1-8
81. Tomie A., Brooks W., and Zito B. In: Klein SB M.R. (Ed). Sign-tracking: the search for reward in Contemporary learning theories (1989), Lawrence Erlbaum Associates, Hillside, NJ 191-223
82. Altman J., Everitt B.J., Glautier S., Markou A., Nutt D., Oretti R., et al. The biological, social and clinical bases of drug addiction: commentary and debate. Psychopharmacology (Berl) 125 4 (1996) 285-345
83. Davey G.C., and Cleland G.G. Topography of signal-centered behavior in the rat: effects of deprivation state and reinforcer type. J Exp Anal Behav 38 3 (1982) 291-304
84. Ito R., Everitt B.J., and Robbins T.W. The hippocampus and appetitive Pavlovian conditioning: effects of excitotoxic hippocampal lesions on conditioned locomotor activity and autoshaping. Hippocampus 15 6 (2005) 713-721
85. Cardinal R.N., Parkinson J.A., Marbini H.D., Toner A.J., Bussey T.J., Robbins T.W., et al. Role of the anterior cingulate cortex in the control over behavior by Pavlovian conditioned stimuli in rats. Behav Neurosci 117 3 (2003) 566-587
86. Bussey T.J., Everitt B.J., and Robbins T.W. Dissociable effects of cingulate and medial frontal cortex lesions on stimulus-reward learning using a novel Pavlovian autoshaping procedure for the rat: implications for the neurobiology of emotion. Behav Neurosci 111 5 (1997) 908-919
87. Bussey T.J., Muir J.L., Everitt B.J., and Robbins T.W. Dissociable effects of anterior and posterior cingulate cortex lesions on the acquisition of a conditional visual discrimination: facilitation of early learning vs. impairment of late learning. Behav Brain Res 82 1 (1996) 45-56
88. Parkinson J.A., Robbins T.W., and Everitt B.J. Dissociable roles of the central and basolateral amygdala in appetitive emotional learning. Eur J Neurosci 12 1 (2000) 405-413
89. Fields H.L., Hjelmstad G.O., Margolis E.B., and Nicola S.M. Ventral tegmental area neurons in learned appetitive behavior and positive reinforcement. Annu Rev Neurosci 30 (2007) 289-316
90. Mirenowicz J., and Schultz W. Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli. Nature 379 6564 (1996) 449-451
91. Schultz W., Tremblay L., and Hollerman J.R. Reward prediction in primate basal ganglia and frontal cortex. Neuropharmacology 37 4-5 (1998) 421-429
92. Hyman S.E., Malenka R.C., and Nestler E.J. Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 29 (2006) 565-598
93. Han J.S., McMahan R.W., Holland P., and Gallagher M. The role of an amygdalo-nigrostriatal pathway in associative learning. J Neurosci 17 10 (1997) 3913-3919
94. Uslaner J.M., Acerbo M.J., Jones S.A., and Robinson T.E. The attribution of incentive salience to a stimulus that signals an intravenous injection of cocaine. Behav Brain Res 169 2 (2006) 320-324
95. Kearns D.N., and Weiss S.J. Sign-tracking (autoshaping) in rats: a comparison of cocaine and food as unconditioned stimuli. Learn Behav 32 4 (2004) 463-476
96. Harmer C.J., and Phillips G.D. Enhanced dopamine efflux in the amygdala by a predictive, but not a non-predictive, stimulus: facilitation by prior repeated D-amphetamine. Neuroscience 90 1 (1999) 119-130
97. Estes W. Discriminative conditioning. II. Effects of a Pavlovian conditioned stimulus upon a subsequently established operant response. J Exp Psychol 38 (1948) 173-177
98. Lovibond P.F. Facilitation of instrumental behavior by a Pavlovian appetitive conditioned stimulus. J Exp Psychol Anim Behav Process 9 3 (1983) 225-247
99. Corbit L.H., and Balleine B.W. Double dissociation of basolateral and central amygdala lesions on the general and outcome-specific forms of pavlovian-instrumental transfer. J Neurosci 25 4 (2005) 962-970
100. Corbit L.H., Janak P.H., and Balleine B.W. General and outcome-specific forms of Pavlovian-instrumental transfer: the effect of shifts in motivational state and inactivation of the ventral tegmental area. Eur J Neurosci 26 11 (2007) 3141-3149
101. Holland P.C., and Gallagher M. Double dissociation of the effects of lesions of basolateral and central amygdala on conditioned stimulus-potentiated feeding and Pavlovian-instrumental transfer. Eur J Neurosci 17 8 (2003) 1680-1694
102. Lovibond P.F. Appetitive Pavlovian-instrumental interactions: effects of inter-stimulus interval and baseline reinforcement conditions. Q J Exp Psychol B 33 Pt 4 (1981) 257-269
103. Holland P.C. Relations between Pavlovian-instrumental transfer and reinforcer devaluation. J Exp Psychol Anim Behav Process 30 2 (2004) 104-117
104. Blundell P., Hall G., and Killcross S. Lesions of the basolateral amygdala disrupt selective aspects of reinforcer representation in rats. J Neurosci 21 22 (2001) 9018-9026
105. Murschall A., and Hauber W. Inactivation of the ventral tegmental area abolished the general excitatory influence of Pavlovian cues on instrumental performance. Learn Mem 13 2 (2006) 123-126
106. Wyvell C.L., and Berridge K.C. Intra-accumbens amphetamine increases the conditioned incentive salience of sucrose reward: enhancement of reward "wanting" without enhanced "liking" or response reinforcement. J Neurosci 20 21 (2000) 8122-8130
107. El-Amamy H., and Holland P.C. Dissociable effects of disconnecting amygdala central nucleus from the ventral tegmental area or substantia nigra on learned orienting and incentive motivation. Eur J Neurosci 25 5 (2007) 1557-1567
108. Corbit L.H., and Janak P.H. Inactivation of the lateral but not medial dorsal striatum eliminates the excitatory impact of Pavlovian stimuli on instrumental responding. J Neurosci 27 51 (2007) 13977-13981
109. Ikemoto S. Involvement of the olfactory tubercle in cocaine reward: intracranial self-administration studies. J Neurosci 23 28 (2003) 9305-9311
110. Hogarth L., Dickinson A., Wright A., Kouvaraki M., and Duka T. The role of drug expectancy in the control of human drug seeking. J Exp Psychol Anim Behav Process 33 4 (2007) 484-496
111. Di Ciano P., Blaha C.D., and Phillips A.G. Conditioned changes in dopamine oxidation currents in the nucleus accumbens of rats by stimuli paired with self-administration or yoked-administration of d-amphetamine. Eur J Neurosci 10 3 (1998) 1121-1127
112. Ito R., Dalley J.W., Howes S.R., Robbins T.W., and Everitt B.J. Dissociation in conditioned dopamine release in the nucleus accumbens core and shell in response to cocaine cues and during cocaine-seeking behavior in rats. J Neurosci 20 19 (2000) 7489-7495
113. Gratton A., and Wise R.A. Drug- and behavior-associated changes in dopamine-related electrochemical signals during intravenous cocaine self-administration in rats. J Neurosci 14 7 (1994) 4130-4146
114. Neisewander J.L., O'Dell L.E., Tran-Nguyen L.T., Castaneda E., and Fuchs R.A. Dopamine overflow in the nucleus accumbens during extinction and reinstatement of cocaine self-administration behavior. Neuropsychopharmacology 15 5 (1996) 506-514
115. Weiss F., Maldonado-Vlaar C.S., Parsons L.H., Kerr T.M., Smith D.L., and 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 8 (2000) 4321-4326
116. Di Ciano P., and Everitt B.J. Differential control over drug-seeking behavior by drug-associated conditioned reinforcers and discriminative stimuli predictive of drug availability. Behav Neurosci 117 5 (2003) 952-960
117. Grimm J.W., Kruzich P.J., and See R.E. Contingent access to stimuli associated with cocaine self-administration is required for reinstatement of drug-seeking behavior. Psychobiology 28 3 (2000) 383-386
118. Corbit L.H., and Janak P.H. Ethanol-associated cues produce general pavlovian-instrumental transfer. Alcohol Clin Exp Res 31 5 (2007) 766-774
119. Robinson T.E., and Berridge K.C. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev 18 3 (1993) 247-291
120. Flagel S.B., Watson S.J., Akil H., and Robinson T.E. Individual differences in the attribution of incentive salience to a reward-related cue: influence on cocaine sensitization. Behav Brain Res 186 1 (2008) 48-56
121. Di Ciano P., and Everitt B.J. Conditioned reinforcing properties of stimuli paired with self-administered cocaine, heroin or sucrose: implications for the persistence of addictive behaviour. Neuropharmacology 47 Suppl. 1 (2004) 202-213
122. Everitt B.J., and Robbins T.W. Second-order schedules of drug reinforcement in rats and monkeys: measurement of reinforcing efficacy and drug-seeking behaviour. Psychopharmacology (Berl) 153 1 (2000) 17-30
123. Robbins T.W. Relationship between reward-enhancing and stereotypical effects of psychomotor stimulant drugs. Nature 264 5581 (1976) 57-59
124. Williams B.A., and Dunn R. Substitutability between conditioned and primary reinforcers in discrimination acquisition. J Exp Anal Behav 55 1 (1991) 21-35
125. Williams B.A. Inverse relations between preference and contrast. J Exp Anal Behav 58 2 (1992) 303-312
126. Goldberg S.R., and Gardner M.L. Second-order schedules: extended sequences of behavior controlled by brief environmental stimuli associated with drug self-administration. NIDA Res Monogr 37 (1981) 241-270
127. Goldberg S.R., Kelleher R.T., and Morse W.H. Second-order schedules of drug injection. Fed Proc 34 9 (1975) 1771-1776
128. Goldberg S.R., Morse W.H., and Goldberg D.M. Behavior maintained under a second-order schedule by intramuscular injection of morphine or cocaine in rhesus monkeys. J Pharmacol Exp Ther 199 1 (1976) 278-286
129. Cador M., Robbins T.W., and Everitt B.J. Involvement of the amygdala in stimulus-reward associations: interaction with the ventral striatum. Neuroscience 30 1 (1989) 77-86
130. Burns L.H., Robbins T.W., and Everitt B.J. Differential effects of excitotoxic lesions of the basolateral amygdala, ventral subiculum and medial prefrontal cortex on responding with conditioned reinforcement and locomotor activity potentiated by intra-accumbens infusions of D-amphetamine. Behav Brain Res 55 2 (1993) 167-183
131. Everitt B.J., Cador M., and Robbins T.W. Interactions between the amygdala and ventral striatum in stimulus-reward associations: studies using a second-order schedule of sexual reinforcement. Neuroscience 30 1 (1989) 63-75
132. Pears A., Parkinson J.A., Hopewell L., Everitt B.J., and Roberts A.C. Lesions of the orbitofrontal but not medial prefrontal cortex disrupt conditioned reinforcement in primates. J Neurosci 23 35 (2003) 11189-11201
133. Cousens G.A., and Otto T. Neural substrates of olfactory discrimination learning with auditory secondary reinforcement. I. Contributions of the basolateral amygdaloid complex and orbitofrontal cortex. Integr Physiol Behav Sci 38 4 (2003) 272-294
134. Burke K.A., Franz T.M., Miller D.N., and Schoenbaum G. The role of the orbitofrontal cortex in the pursuit of happiness and more specific rewards. Nature 454 7202 (2008) 340-344
135. Robbins T.W. Reward enhancement by psychomotor stimulant drugs [proceedings]. Neuropharmacology 16 7-8 (1977) 529-530
136. Taylor J.R., and Robbins T.W. Enhanced behavioural control by conditioned reinforcers following microinjections of d-amphetamine into the nucleus accumbens. Psychopharmacology (Berl) 84 3 (1984) 405-412
137. Taylor J.R., and Horger B.A. Enhanced responding for conditioned reward produced by intra-accumbens amphetamine is potentiated after cocaine sensitisation. Psychopharmacology (Berl) 142 1 (1999) 31-40
138. Robbins T.W., Cador M., Taylor J.R., and Everitt B.J. Limbic-striatal interactions in reward-related processes. Neurosci Biobehav Rev 13 2-3 (1989) 155-162
139. Taylor J.R., and Robbins T.W. 6-Hydroxydopamine lesions of the nucleus accumbens, but not of the caudate nucleus, attenuate enhanced responding with reward-related stimuli produced by intra-accumbens d-amphetamine. Psychopharmacology (Berl) 90 3 (1986) 390-397
140. Wolterink G., Phillips G., Cador M., Donselaar-Wolterink I., Robbins T.W., and Everitt B.J. Relative roles of ventral striatal D1 and D2 dopamine receptors in responding with conditioned reinforcement. Psychopharmacology (Berl) 110 3 (1993) 355-364
141. Di Ciano P., and Everitt B.J. Neuropsychopharmacology of drug seeking: Insights from studies with second-order schedules of drug reinforcement. Eur J Pharmacol 526 1-3 (2005) 186-198
142. Arroyo M., Markou A., Robbins T.W., and Everitt B.J. Acquisition, maintenance and reinstatement of intravenous cocaine self-administration under a second-order schedule of reinforcement in rats: effects of conditioned cues and continuous access to cocaine. Psychopharmacology (Berl) 140 3 (1998) 331-344
143. Di Ciano P., and Everitt B.J. Direct interactions between the basolateral amygdala and nucleus accumbens core underlie cocaine-seeking behavior by rats. J Neurosci 24 32 (2004) 7167-7173
144. Goldberg S.R. Comparable behavior maintained under fixed-ratio and second-order schedules of food presentation, cocaine injection or d-amphetamine injection in the squirrel monkey. J Pharmacol Exp Ther 186 1 (1973) 18-30
145. Goldberg S.R., Spealman R.D., and Kelleher R.T. Enhancement of drug-seeking behavior by environmental stimuli associated with cocaine or morphine injections. Neuropharmacology 18 12 (1979) 1015-1017
146. Goldberg S.T., and Kelleher R.T. Behavior controlled by scheduled injections of cocaine in squirrel and rhesus monkeys. J Exp Anal Behav 25 1 (1976) 93-104
147. Henningfield J.E., Nemeth-Coslett R., Katz J.L., and Goldberg S.R. Intravenous cocaine self-administration by human volunteers: second-order schedules of reinforcement. NIDA Res Monogr 76 (1987) 266-273
148. Kelleher R.T., and Goldberg S.R. Fixed-interval responding under second-order schedules of food presentation or cocaine injection. J Exp Anal Behav 28 3 (1977) 221-231
149. Goldberg S.R., Spealman R.D., and Goldberg D.M. Persistent behavior at high rates maintained by intravenous self-administration of nicotine. Science 214 4520 (1981) 573-575
150. Di Ciano P., and Everitt B.J. Dissociable effects of antagonism of NMDA and AMPA/KA receptors in the nucleus accumbens core and shell on cocaine-seeking behavior. Neuropsychopharmacology 25 3 (2001) 341-360
151. Alderson H.L., Robbins T.W., and Everitt B.J. Heroin self-administration under a second-order schedule of reinforcement: acquisition and maintenance of heroin-seeking behaviour in rats. Psychopharmacology (Berl) 153 1 (2000) 120-133
152. Lee J.L., Milton A.L., and Everitt B.J. Cue-induced cocaine seeking and relapse are reduced by disruption of drug memory reconsolidation. J Neurosci 26 22 (2006) 5881-5887
153. Goldberg S.R., Kelleher R.T., and Goldberg D.M. Fixed-ratio responding under second-order schedules of food presentation or cocaine injection. J Pharmacol Exp Ther 218 1 (1981) 271-281
154. Whitelaw R.B., Markou A., Robbins T.W., and Everitt B.J. Excitotoxic lesions of the basolateral amygdala impair the acquisition of cocaine-seeking behaviour under a second-order schedule of reinforcement. Psychopharmacology (Berl) 127 3 (1996) 213-224
155. Hutcheson D.M., and Everitt B.J. The effects of selective orbitofrontal cortex lesions on the acquisition and performance of cue-controlled cocaine seeking in rats. Ann N Y Acad Sci 1003 (2003) 410-411
156. Everitt B.J., Hutcheson D.M., Ersche K.D., Pelloux Y., Dalley J.W., and Robbins T.W. The orbital prefrontal cortex and drug addiction in laboratory animals and humans. Ann N Y Acad Sci 1121 (2007) 576-597
157. Di Ciano P., and Everitt B.J. Contribution of the ventral tegmental area to cocaine-seeking maintained by a drug-paired conditioned stimulus in rats. Eur J Neurosci 19 6 (2004) 1661-1667
158. 3 receptors in the basolateral amygdala. Behav Neurosci 122 1 (2008) 129-139
159. Ito R., Dalley J.W., Robbins T.W., and Everitt B.J. Dopamine release in the dorsal striatum during cocaine-seeking behavior under the control of a drug-associated cue. J Neurosci 22 14 (2002) 6247-6253
160. Letchworth S.R., Nader M.A., Smith H.R., Friedman D.P., and Porrino L.J. Progression of changes in dopamine transporter binding site density as a result of cocaine self-administration in rhesus monkeys. J Neurosci 21 8 (2001) 2799-2807
161. Porrino L.J., Lyons D., Smith H.R., Daunais J.B., and Nader M.A. Cocaine self-administration produces a progressive involvement of limbic, association, and sensorimotor striatal domains. J Neurosci 24 14 (2004) 3554-3562
162. Ikemoto S. Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res Rev 56 1 (2007) 27-78
163. Yin H.H., and Knowlton B.J. The role of the basal ganglia in habit formation. Nat Rev Neurosci 7 6 (2006) 464-476
164. Everitt B.J., and Wolf M.E. Psychomotor stimulant addiction: a neural systems perspective. J Neurosci 22 9 (2002) 3312-3320
165. Shaham Y., Shalev U., Lu L., De Wit H., and Stewart J. The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology (Berl) 168 1-2 (2003) 3-20
166. Kruzich P.J., and See R.E. Differential contributions of the basolateral and central amygdala in the acquisition and expression of conditioned relapse to cocaine-seeking behavior. J Neurosci 21 14 (2001) pRC155
167. Backstrom P., and Hyytia P. Involvement of AMPA/kainate, NMDA, and mGlu5 receptors in the nucleus accumbens core in cue-induced reinstatement of cocaine seeking in rats. Psychopharmacology (Berl) 192 4 (2007) 571-580
168. Lu L., Dempsey J., Shaham Y., and Hope B.T. Differential long-term neuroadaptations of glutamate receptors in the basolateral and central amygdala after withdrawal from cocaine self-administration in rats. J Neurochem 94 1 (2005) 161-168
169. Deroche V., Le Moal M., and Piazza P.V. Cocaine self-administration increases the incentive motivational properties of the drug in rats. Eur J Neurosci 11 8 (1999) 2731-2736
170. Ahmed S.H., and Cador M. Dissociation of psychomotor sensitization from compulsive cocaine consumption. Neuropsychopharmacology 31 3 (2006) 563-571
171. Reep R.L., Cheatwood J.L., and Corwin J.V. The associative striatum: organization of cortical projections to the dorsocentral striatum in rats. J Comp Neurol 467 3 (2003) 271-292
172. Kelley A.E., Domesick V.B., and Nauta W.J. The amygdalostriatal projection in the rat-an anatomical study by anterograde and retrograde tracing methods. Neuroscience 7 3 (1982) 615-630
173. Redgrave P., and Gurney K. The short-latency dopamine signal: a role in discovering novel actions?. Nat Rev Neurosci 7 12 (2006) 967-975
174. Schultz W. Predictive reward signal of dopamine neurons. J Neurophysiol 80 1 (1998) 1-27
175. Schultz W. The reward signal of midbrain dopamine neurons. News Physiol Sci 14 (1999) 249-255
176. Schultz W. Reward signaling by dopamine neurons. Neuroscientist 7 4 (2001) 293-302
177. Schultz W. Behavioral dopamine signals. Trends Neurosci 30 5 (2007) 203-210
178. Schultz W., Dayan P., and Montague P.R. A neural substrate of prediction and reward. Science 275 5306 (1997) 1593-1599
179. Schultz W., and Dickinson A. Neuronal coding of prediction errors. Annu Rev Neurosci 23 (2000) 473-500
180. Robinson T.E., and Berridge K.C. The psychology and neurobiology of addiction: an incentive-sensitization view. Addiction 95 Suppl. 2 (2000) S91-117
181. Robinson T.E., and Berridge K.C. Incentive-sensitization and addiction. Addiction 96 1 (2001) 103-114
182. Koob G.F., and Le Moal M. Drug abuse: hedonic homeostatic dysregulation. Science 278 5335 (1997) 52-58
183. Koob G.F., and Le Moal M. Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24 2 (2001) 97-129
184. Koob G.F., and Le Moal M. Plasticity of reward neurocircuitry and the 'dark side' of drug addiction. Nat Neurosci 8 11 (2005) 1442-1444
185. Diagnostic and statistical manual of mental disorders (ed 4, revised version 2000) (2000), American Psychiatric Association
186. Kirby K.N., Petry N.M., and Bickel W.K. Heroin addicts have higher discount rates for delayed rewards than non-drug-using controls. J Exp Psychol Gen 128 1 (1999) 78-87
187. Hester R., and Garavan H. Executive dysfunction in cocaine addiction: evidence for discordant frontal, cingulate, and cerebellar activity. J Neurosci 24 49 (2004) 11017-11022
188. Moeller F.G., Dougherty D.M., Barratt E.S., Oderinde V., Mathias C.W., Harper R.A., et al. Increased impulsivity in cocaine dependent subjects independent of antisocial personality disorder and aggression. Drug Alcohol Depend 68 1 (2002) 105-111
189. Dom G., D'Haene P., Hulstijn W., and Sabbe B. Impulsivity in abstinent early- and late-onset alcoholics: differences in self-report measures and a discounting task. Addiction 101 1 (2006) 50-59
190. Paine T.A., Dringenberg H.C., and Olmstead M.C. Effects of chronic cocaine on impulsivity: relation to cortical serotonin mechanisms. Behav Brain Res 147 1-2 (2003) 135-147
191. Calu D.J., Stalnaker T.A., Franz T.M., Singh T., Shaham Y., and Schoenbaum G. Withdrawal from cocaine self-administration produces long-lasting deficits in orbitofrontal-dependent reversal learning in rats. Learn Mem 14 5 (2007) 325-328
192. Black Y.D., Maclaren F.R., Naydenov A.V., Carlezon Jr. W.A., Baxter M.G., and Konradi C. Altered attention and prefrontal cortex gene expression in rats after binge-like exposure to cocaine during adolescence. J Neurosci 26 38 (2006) 9656-9665
193. George O., Mandyam C.D., Wee S., and Koob G.F. Extended access to cocaine self-administration produces long-lasting prefrontal cortex-dependent working memory impairments. Neuropsychopharmacology 33 10 (2008) 2474-2482
194. Dalley J.W., Theobald D.E., Berry D., Milstein J.A., Laane K., Everitt B.J., et al. Cognitive sequelae of intravenous amphetamine self-administration in rats: evidence for selective effects on attentional performance. Neuropsychopharmacology 30 3 (2005) 525-537
195. Dalley J.W., Laane K., Pena Y., Theobald D.E., Everitt B.J., and Robbins T.W. Attentional and motivational deficits in rats withdrawn from intravenous self-administration of cocaine or heroin. Psychopharmacology (Berl) 182 4 (2005) 579-587
196. Paine T.A., and Olmstead M.C. Cocaine disrupts both behavioural inhibition and conditional discrimination in rats. Psychopharmacology (Berl) 175 4 (2004) 443-450
197. Schoenbaum G., Saddoris M.P., Ramus S.J., Shaham Y., and Setlow B. Cocaine-experienced rats exhibit learning deficits in a task sensitive to orbitofrontal cortex lesions. Eur J Neurosci 19 7 (2004) 1997-2002
198. Schoenbaum G., and Roesch M. Orbitofrontal cortex, associative learning, and expectancies. Neuron 47 5 (2005) 633-636
199. Schoenbaum G., Roesch M.R., and Stalnaker T.A. Orbitofrontal cortex, decision-making and drug addiction. Trends Neurosci 29 2 (2006) 116-124
200. Schoenbaum G., Setlow B., Saddoris M.P., and Gallagher M. Encoding predicted outcome and acquired value in orbitofrontal cortex during cue sampling depends upon input from basolateral amygdala. Neuron 39 5 (2003) 855-867
201. Schoenbaum G., and Shaham Y. The role of orbitofrontal cortex in drug addiction: a review of preclinical studies. Biol Psychiatry 63 3 (2008) 256-262
202. Bolla K.I., Eldreth D.A., London E.D., Kiehl K.A., Mouratidis M., Contoreggi C., et al. Orbitofrontal cortex dysfunction in abstinent cocaine abusers performing a decision-making task. Neuroimage 19 3 (2003) 1085-1094
203. Jentsch J.D., and Taylor J.R. Impulsivity resulting from frontostriatal dysfunction in drug abuse: implications for the control of behavior by reward-related stimuli. Psychopharmacology (Berl) 146 4 (1999) 373-390
204. Porrino L.J., Smith H.R., Nader M.A., and Beveridge T.J. The effects of cocaine: a shifting target over the course of addiction. Prog Neuropsychopharmacol Biol Psychiatry 31 8 (2007) 1593-1600
205. Volkow N.D., Fowler J.S., Wang G.J., Hitzemann R., Logan J., Schlyer D.J., et al. Decreased dopamine D2 receptor availability is associated with reduced frontal metabolism in cocaine abusers. Synapse 14 2 (1993) 169-177
206. Dalley J.W., Cardinal R.N., and Robbins T.W. Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neurosci Biobehav Rev 28 7 (2004) 771-784
207. Tanji J., and Hoshi E. Role of the lateral prefrontal cortex in executive behavioral control. Physiol Rev 88 1 (2008) 37-57
208. Muller J., Dreisbach G., Goschke T., Hensch T., Lesch K.P., and Brocke B. Dopamine and cognitive control: the prospect of monetary gains influences the balance between flexibility and stability in a set-shifting paradigm. Eur J Neurosci 26 12 (2007) 3661-3668
209. Koechlin E., and Summerfield C. An information theoretical approach to prefrontal executive function. Trends Cogn Sci 11 6 (2007) 229-235
210. Goldstein R.Z., and Volkow N.D. Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. Am J Psychiatry 159 10 (2002) 1642-1652
211. Dalley J.W., Fryer T.D., Brichard L., Robinson E.S., Theobald D.E., Laane K., et al. Nucleus accumbens D2/3 receptors predict trait impulsivity and cocaine reinforcement. Science 315 5816 (2007) 1267-1270
212. Belin D., Mar A.C., Dalley J.W., Robbins T.W., and Everitt B.J. High impulsivity predicts the switch to compulsive cocaine-taking. Science 320 5881 (2008) 1352-1355