Individual differences in the attribution of incentive salience to reward-related cues: Implications for addiction

Neuropharmacology

Volumn 56, Issue SUPPL. 1, 2009, Pages 139-148

  Flagel, Shelly B ^a   Akil, Huda ^a   Robinson, Terry E ^b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Addiction; Autoshaping; Goal tracking; Incentive salience; Pavlovian conditioning; Sign tracking

Indexed keywords

COCAINE;

ADDICTION; ASSOCIATION; CONDITIONING; HUMAN; INDIVIDUALITY; MOTIVATION; NEUROBIOLOGY; NONHUMAN; PLACE PREFERENCE; PRIORITY JOURNAL; REVIEW; REWARD; STRESS;

ANIMALS; BEHAVIOR, ADDICTIVE; CUES; HUMANS; INDIVIDUALITY; MOTIVATION; REWARD;

EID: 58049181065     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2008.06.027     Document Type: Review

References (118)

1. Anagnostaras S.G., and Robinson T.E. Sensitization to the psychomotor stimulant effects of amphetamine: modulation by associative learning. Behav. Neurosci. 110 (1996) 1397-1414
2. Anagnostaras S.G., Schallert T., and Robinson T.E. Memory processes governing amphetamine-induced psychomotor sensitization. Neuropsychopharmacology 26 (2002) 703-715
3. Bardo M.T., and Bevins R.A. Conditioned place preference: what does it add to our preclinical understanding of drug reward?. Psychopharmacology (Berl) 153 (2000) 31-43
4. 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 (2008) 1352-1355
5. Berridge K.C. Food reward: brain substrates of wanting and liking. Neurosci. Biobehav. Rev. 20 (1996) 1-25
6. Berridge K.C. Reward learning: reinforcement, incentives and expectations. In: Medin D. (Ed). Psychology of learning and motivation (2001), Academic Press 223-278
7. Berridge K.C., and Robinson T.E. Parsing reward. Trends Neurosci. 26 (2003) 507-513
8. Bindra D. How adaptive behavior is produced: a perceptual-motivation alternative to response reinforcement. Behav. Brain Sci. 1 (1978) 41-91
9. Boakes R. Performance on learning to associate a stimulus with positive reinforcement. In: Davis H., and Hurwitz H. (Eds). Operant-Pavlovian Interactions (1977), Erlbaum, Hillsdale, NJ 67-97
10. Boakes R.A., Poli M., Lockwood M.J., and Goodall G. A study of misbehavior: token reinforcement in the rat. J. Exp. Anal. Behav. 29 (1978) 115-134
11. Bolles R.C. Reinforcement, expectancy, and learning. Psychol. Rev. 79 (1972) 394-409
12. Boughner R.L., and Papini M.R. Appetitive latent inhibition in rats: now you see it (sign tracking), now you don't (goal tracking). Learn Behav. 31 (2003) 387-392
13. Breland K., and Breland M. The misbehavior of organisms. Am. Psychol. 16 (1961) 681-683
14. Breland K., and Breland M. Animal Behavior (1966), Macmillan, New York
15. Brown B., Hemmes N., de Vaca S.C., and Pagano C. Sign and goal tracking during delay and trace autoshaping in pigeons. Anim. Learn Behav. 21 (1993) 360-368
16. Brown P.L., and Jenkins H.M. Auto-shaping of the pigeon's key-peck. J. Exp. Anal. Behav. 11 (1968) 1-8
17. Burns M., and Domjan M. Sign tracking versus goal tracking in the sexual conditioning of male Japanese quail (Coturnix japonica). J. Exp. Psychol. Anim. Behav. Process. 22 (1996) 297-306
18. Burns M., and Domjan M. Topography of spatially directed conditioned responding: effects of context and trial duration. J. Exp. Psychol. Anim. Behav. Process. 27 (2001) 269-278
19. Buzsaki G. The "where is it?" reflex: autoshaping the orienting response. J. Exp. Anal. Behav. 37 (1982) 461-484
20. Cardinal R.N., and Everitt B.J. Neural and psychological mechanisms underlying appetitive learning: links to drug addiction. Curr. Opin. Neurobiol. 14 (2004) 156-162
21. 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 (2002) 321-352
22. Cardinal R.N., Parkinson J.A., Lachenal G., Halkerston K.M., Rudarakanchana N., Hall J., Morrison C.H., Howes S.R., Robbins T.W., and Everitt B.J. 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 (2002) 553-567
23. Carr G., Fibiger H., and Phillips A. Conditioned place preference as a measure of drug reward. In: Liebman J., and Cooper S. (Eds). The Neuropharmacological Basis of Reward (1989), Oxford University Press 264-319
24. Childress A.R., Ehrman R., Rohsenow D., Robbins S.J., and O'Brien C.P. Classically conditioned factors in drug dependence. In: Lowinson J., and Millman R.P. (Eds). Comprehensive Textbook of Substance Abuse (1993), Williams and Wilkins, Baltimore 56-69
25. Ciccocioppo R., Martin-Fardon R., and Weiss F. Stimuli associated with a single cocaine experience elicit long-lasting cocaine-seeking. Nat. Neurosci. 7 (2004) 495-496
26. Cleland G.G., and Davey G.C. Autoshaping in the rat: the effects of localizable visual and auditory signals for food. J. Exp. Anal. Behav. 40 (1983) 47-56
27. Corbit L.H., and Janak P.H. Ethanol-associated cues produce general pavlovian-instrumental transfer. Alcohol. Clin. Exp. Res. 31 (2007) 766-774
28. Costa D.S., and Boakes R.A. Maintenance of responding when reinforcement becomes delayed. Learn Behav. 35 (2007) 95-105
29. Crombag H.S., and Shaham Y. Renewal of drug seeking by contextual cues after prolonged extinction in rats. Behav. Neurosci. 116 (2002) 169-173
30. Cunningham C.L., and Patel P. Rapid induction of Pavlovian approach to an ethanol-paired visual cue in mice. Psychopharmacology (Berl) 192 (2007) 231-241
31. Cunningham C.L., Patel P., and Milner L. Spatial location is critical for conditioning place preference with visual but not tactile stimuli. Behav. Neurosci. 120 (2006) 1115-1132
32. Dalley J.W., Laane K., Theobald D.E., Armstrong H.C., Corlett P.R., Chudasama Y., and Robbins T.W. Time-limited modulation of appetitive Pavlovian memory by D1 and NMDA receptors in the nucleus accumbens. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 6189-6194
33. 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 (1982) 291-304
34. Davey G.C., Cleland G.G., Oakley D.A., and Jacobs J.L. The effect of early feeding experience on signal-directed response topography in the rat. Physiol. Behav. 32 (1984) 11-15
35. Davey G.C., Oakley D., and Cleland G.G. Autoshaping in the rat: effects of omission on the form of the response. J. Exp. Anal. Behav. 36 (1981) 75-91
36. Day J.J., and Carelli R.M. The nucleus accumbens and Pavlovian reward learning. Neuroscientist 13 (2007) 148-159
37. Day J.J., Wheeler R.A., Roitman M.F., and Carelli R.M. Nucleus accumbens neurons encode Pavlovian approach behaviors: evidence from an autoshaping paradigm. Eur. J. Neurosci. 23 (2006) 1341-1351
38. DeJong W. Relapse prevention: an emerging technology for promoting long-term drug abstinence. Int. J. Addict. 29 (1994) 681-705
39. Di Chiara G. A motivational learning hypothesis of the role of mesolimbic dopamine in compulsive drug use. J. Psychopharmacol. 12 (1998) 54-67
40. 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
41. Dickinson A., Smith J., and Mirenowicz J. Dissociation of Pavlovian and instrumental incentive learning under dopamine antagonists. Behav. Neurosci. 114 (2000) 468-483
42. Domjan M., O'Vary D., and Greene P. Conditioning of appetitive and consummatory sexual behavior in male Japanese quail. J. Exp. Anal. Behav. 50 (1988) 505-519
43. Engberg L.A., Hansen G., Welker R.L., and Thomas D.R. Acquisition of key-pecking via autoshaping as a function of prior experience: "learned laziness"?. Science 178 (1972) 1002-1004
44. 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 (2000) 17-30
45. Everitt B.J., and Robbins T.W. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat. Neurosci. 8 (2005) 1481-1489
46. Farwell B.J., and Ayres J.J.B. Stimulus-reinforcer and response-reinforcer relations in the control of conditioned appetitive headpoking ("goal-tracking") in rats. Learn Motiv. 10 (1979) 295-312
47. 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 (2008) 48-56
48. Flagel S.B., Watson S.J., Robinson T.E., and Akil H. An animal model of individual differences in "conditionability": relevance to psychopathology. Neuropsychopharmacology 31 (2006) S262-S263
49. Flagel S.B., Watson S.J., Robinson T.E., and Akil H. Individual differences in the propensity to approach signals vs goals promote different adaptations in the dopamine system of rats. Psychopharmacology (Berl) 191 (2007) 599-607
50. Gamzu E., and Williams D.R. Classical conditioning of a complex skeletal response. Science 171 (1971) 923-925
51. Hearst E., and Jenkins H. Sign-tracking: the Stimulus-reinforcer Relation and Directed Action (1974), Monograph of the Psychonomic Society, Austin
52. Holland P.C. Conditioned stimulus as a determinant of the form of the Pavlovian conditioned response. J. Exp. Psychol. Anim. Behav. Process. 3 (1977) 77-104
53. Holland P.C. CS-US interval as a determinant of the form of Pavlovian appetitive conditioned responses. J. Exp. Psychol. Anim. Behav. Process. 6 (1980) 155-174
54. Holland P.C. Influence of visual conditioned stimulus characteristics on the form of Pavlovian appetitive conditioned responding in rats. J. Exp. Psychol. Anim. Behav. Process. 6 (1980) 81-97
55. Holland P.C. Occasion setting in Pavlovian conditioning. In: Medin D.L. (Ed). The Psychology of Learning and Motivation (1992), Academic Press, San Diego 69-125
56. Jenkins H.M., and Moore B.R. The form of the auto-shaped response with food or water reinforcers. J. Exp. Anal. Behav. 20 (1973) 163-181
57. Kearns D.N., Gomez-Serrano M.A., Weiss S.J., and Riley A.L. A comparison of Lewis and Fischer rat strains on autoshaping (sign-tracking), discrimination reversal learning and negative auto-maintenance. Behav. Brain Res. 169 (2006) 193-200
58. Kearns D.N., and Weiss S.J. Sign-tracking (autoshaping) in rats: a comparison of cocaine and food as unconditioned stimuli. Learn Behav. 32 (2004) 463-476
59. Kemenes G., and Benjamin P.R. Goal-tracking behavior in the pond snail, Lymnaea stagnalis. Behav. Neural Biol. 52 (1989) 260-270
60. Killeen P.R. Complex dynamic processes in sign tracking with an omission contingency (negative automaintenance). J. Exp. Psychol. Anim. Behav. Process. 29 (2003) 49-61
61. Koksal F., Domjan M., Kurt A., Sertel O., Orung S., Bowers R., and Kumru G. An animal model of fetishism. Behav. Res. Ther. 42 (2004) 1421-1434
62. Krank M.D. Pavlovian conditioning with ethanol: sign-tracking (autoshaping), conditioned incentive, and ethanol self-administration. Alcohol. Clin. Exp. Res. 27 (2003) 1592-1598
63. Krank M.D., O'Neill S., Squarey K., and Jacob J. Goal- and signal-directed incentive: conditioned approach, seeking, and consumption established with unsweetened alcohol in rats. Psychopharmacology (Berl) 196 (2008) 397-405
64. Kruzich P.J., Congleton K.M., and See R.E. Conditioned reinstatement of drug-seeking behavior with a discrete compound stimulus classically conditioned with intravenous cocaine. Behav. Neurosci. 115 (2001) 1086-1092
65. Lajoie J., and Bindra D. An interpretation of autoshaping and related phenomena in terms of stimulus-incentive contingencies alone. Can. J. Psychol. 30 (1976) 157-173
66. Locurto C., Terrace H.S., and Gibbon J. Autoshaping, random control, and omission training in the rat. J. Exp. Anal. Behav. 26 (1976) 451-462
67. Locurto C.M. Contributions of autoshaping to the partitioning of conditioned behavior. In: Locurto C.M., Terrace H.S., and Gibbon J. (Eds). Autoshaping and Conditioning Theory (1981), Academic Press, New York 101-135
68. Lovibond P.F. Facilitation of instrumental behavior by a Pavlovian appetitive conditioned stimulus. J. Exp. Psychol. Anim. Behav. Process. 9 (1983) 225-247
69. McAlonan G.M., Robbins T.W., and Everitt B.J. Effects of medial dorsal thalamic and ventral pallidal lesions on the acquisition of a conditioned place preference: further evidence for the involvement of the ventral striatopallidal system in reward-related processes. Neuroscience 52 (1993) 605-620
70. Moore B.R. The role of directed Pavlovian reactions in simple instrumental learning in the pigeon. In: Hinde R.A., and Stevenson-Hinde J. (Eds). Constraints on Learning: Limitations and Predispositions (1973), Academic Press, London
71. Myerson J., Myerson W.A., and Parker B.K. Automaintenance without stimulus-change reinforcement: temporal control of key pecks. J. Exp. Anal. Behav. 31 (1979) 395-403
72. Newlin D.B. A comparison of drug conditioning and craving for alcohol and cocaine. Recent Dev. Alcohol 10 (1992) 147-164
73. Newlin D.B. The self-perceived survival ability and reproductive fitness (SPFit) theory of substance use disorders. Addiction 97 (2002) 427-445
74. Nilsson, J., Kristiansen, T.S., Fosseidengen, J.E., Ferno, A., van den Bos, R. Sign- and goal-tracking in Atlantic cod (Gadus morhua). Anim Cogn, in press, doi:10.1007/s10071-008-0155-2.
75. O'Flaherty W.D. The Gamblers Lament. The Rig Veda: An Anthology (1981), Penguin Books, New York
76. Pavlov I. Conditioned Reflexes: An Investigation of the Physiological Activity of the Cerebral Cortex (1927), Oxford University Press, London
77. Pavlov I. The reply of a physiologist to psychologists. Psychol. Rev. 39 (1932) 91-127
78. Peterson G.B. Response selection properties of food and brain-stimulation reinforcers in rats. Physiol. Behav. 14 (1975) 681-688
79. Peterson G.B., Ackil J.E., Frommer G.P., and Hearst E.S. Conditioned approach and contact behavior toward signals for food or brain-stimulation reinforcement. Science 177 (1972) 1009-1011
80. Phillips A.G., McDonald A.C., and Wilkie D.M. Disruption of autoshaped responding to a signal of brain-stimulation reward by neuroleptic drugs. Pharmacol. Biochem. Behav. 14 (1981) 543-548
81. Purdy J.E., Roberts A.C., and Garcia C.A. Sign tracking in cuttlefish (Sepia officinalis). J. Comp. Psychol. 113 (1999) 443-449
82. Rescorla R.A. Pavlovian conditioning. It's not what you think it is. Am. Psychol. 43 (1988) 151-160
83. Robinson T.E., and Berridge K.C. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res. Rev. 18 (1993) 247-291
84. Sanabria F., Sitomer M.T., and Killeen P.R. Negative automaintenance omission training is effective. J. Exp. Anal. Behav. 86 (2006) 1-10
85. Schindler C.W., Panlilio L.V., and Goldberg S.R. Second-order schedules of drug self-administration in animals. Psychopharmacology (Berl) 163 (2002) 327-344
86. Schmajuk N.A., and Holland P.C. Occasion Setting: Associative Learning and Cognition in Animals (1998), American Psychological Association, Washington, D.C
87. Schwam E., and Gamzu E. Constraints on autoshaping in the squirrel monkey: stimulus and response factors. Bull. Psychonom. Soc. 5 (1975) 369-372
88. 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 (2003) 3-20
89. Silva F.J., Silva K.M., and Pear J.J. Sign- versus goal-tracking: effects of conditioned-stimulus-to-unconditioned-stimulus distance. J. Exp. Anal. Behav. 57 (1992) 17-31
90. Skinner B.F. The Behavior of Organisms (1938), Appleton-Century-Crofts, New York
91. Staddon J.E.R., and Simmelhag V.L. The "superstition" experiment: a reexamination of its implications for the principles of adaptive behavior. Psychol. Rev. 78 (1971) 3-43
92. Stead J.D., Clinton S., Neal C., Schneider J., Jama A., Miller S., Vazquez D.M., Watson S.J., and Akil H. Selective breeding for divergence in novelty-seeking traits: heritability and enrichment in spontaneous anxiety-related behaviors. Behav. Genet. 36 (2006) 697-712
93. Stewart J., de Wit H., and Eikelboom R. Role of unconditioned and conditioned drug effects in the self-administration of opiates and stimulants. Psychol. Rev. 91 (1984) 251-268
94. Stiers M., and Silberberg A. Lever-contact responses in rats: automaintenance with and without a negative response-reinforcer dependency. J. Exp. Anal. Behav. 22 (1974) 497-506
95. Timberlake W., and Grant D.L. Auto-shaping in rats to the presentation of another rat predicting food. Science 190 (1975) 690-692
96. Timberlake W., and Lucas G.A. The basis of superstitious behavior: chance contingency, stimulus substitution, or appetitive behavior?. J. Exp. Anal. Behav. 44 (1985) 279-299
97. Toates F. Motivational Systems (1986), Cambridge University Press, Cambridge, UK
98. Toates F. The interaction of cognitive and stimulus-response processes in the control of behaviour. Neurosci. Biobehav. Rev. 22 (1998) 59-83
99. Tomie A. Locating reward cue at response manipulandum (CAM) induces symptoms of drug abuse. Neurosci. Biobehav. Rev. 20 (1996) 505-535
100. Tomie A. Autoshaping and drug-taking. In: Mowrer R.R., and Klein S.B. (Eds). Handbook of Contemporary Learning Theories (2001), Erlbaum, Hillsdale, NJ 409-439
101. Tomie A., Aguado A.S., Pohorecky L.A., and Benjamin D. Ethanol induces impulsive-like responding in a delay-of-reward operant choice procedure: impulsivity predicts autoshaping. Psychopharmacology (Berl) 139 (1998) 376-382
102. Tomie A., Aguado A.S., Pohorecky L.A., and Benjamin D. Individual differences in pavlovian autoshaping of lever pressing in rats predict stress-induced corticosterone release and mesolimbic levels of monoamines. Pharmacol. Biochem. Behav. 65 (2000) 509-517
103. Tomie A., Brooks W., and Zito B. Sign-tracking: the search for reward. In: Klein S., and Mowrer R. (Eds). Contemporary Learning Theories: Pavlovian Conditioning and the Status of Traditional Learning Theory (1989), Lawrence Erlbaum Associates, Hillsdale, NJ 191-223
104. Tomie A., Festa E.D., Sparta D.R., and Pohorecky L.A. Lever conditioned stimulus-directed autoshaping induced by saccharin-ethanol unconditioned stimulus solution: effects of ethanol concentration and trial spacing. Alcohol 30 (2003) 35-44
105. Tomie, A., Grimes, K.L., Pohorecky, L.A. Behavioral characteristics and neurobiological substrates shared by Pavlovian sign-tracking and drug abuse. Brain Res. Rev., in press, doi:10.1016/j.brainresrev.2007.12.003.
106. Tomie A., Tirado A.D., Yu L., and Pohorecky L.A. Pavlovian autoshaping procedures increase plasma corticosterone and levels of norepinephrine and serotonin in prefrontal cortex in rats. Behav. Brain Res. 153 (2004) 97-105
107. 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 (2006) 320-324
108. Uslaner, J.M., Dell'orco, J.M., Pevzner, A., Robinson, T.E. The influence of subthalamic nucleus lesions on sign-tracking to stimuli paired with food and drug rewards: facilitation of incentive salience attribution? Neuropsychopharmacology, in Press, doi:10.1038/sj.npp.1301653.
109. Wasserman E.A. Pavlovian conditioning with heat reinforcement produces stimulus-directed pecking in chicks. Science 181 (1973) 875-877
110. Wessels M.G. The effects of reinforcement upon the prepecking behaviors of pigeons in the autoshaping experiment. J. Exp. Anal. Behav. 21 (1974) 125-144
111. White N.M. Addictive drugs as reinforcers: multiple partial actions on memory systems. Addiction 91 (1996) 921-949 (discussion 951-965)
112. White N.M., Chai S.C., and Hamdani S. Learning the morphine conditioned cue preference: cue configuration determines effects of lesions. Pharmacol. Biochem. Behav. 81 (2005) 786-796
113. Wilkie D.M., and McDonald A.C. Autoshaping in the rat with electrical stimulation of the brain as the US. Physiol. Behav. 21 (1978) 325-328
114. Williams B.A., and Dunn R. Preference for conditioned reinforcement. J. Exp. Anal. Behav. 55 (1991) 37-46
115. Williams D., and Williams H. Automaintenance in the pigeon: sustained pecking despite contingent non-reinforcement. J. Exp. Anal. Behav. 12 (1969) 511-520
116. 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 (2000) 8122-8130
117. Zamble E., Hadad G.M., Mitchell J.B., and Cutmore T.R. Pavlovian conditioning of sexual arousal: first- and second-order effects. J. Exp. Psychol. Anim. Behav. Process. 11 (1985) 598-610
118. Zener K. The significance of behavior accompanying conditioned salivary secretion for theories of the conditioned response. Am. J. Psychol. (1937) 384-403