The attribution of incentive salience to Pavlovian alcohol cues: A shift from goal-tracking to sign-tracking

Frontiers in Behavioral Neuroscience

Volumn 9, Issue MAR, 2015, Pages

  Srey, Chandra S ^a   Maddux, Jean Marie N ^a   Nadia, Chaudhri ^a  

^a Department of Psychology Center for Studies in Behavioral Neurobiology/FRQS Groupe de Recherche en Neurobiologie Comportementale Concordia University ^*  (Canada)

Author keywords

Autoshaping; Conditioned reinforcement; Conditioned stimulus; Ethanol; Motivation; Rat

Indexed keywords

ALCOHOL;

ALCOHOL CONSUMPTION; ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; CONDITIONED REFLEX; CONTROLLED STUDY; DRINKING BEHAVIOR; GOAL ATTAINMENT; HABITUATION; INSTRUMENTAL CONDITIONING; LEARNING; MALE; NONHUMAN; RAT; REINFORCEMENT; STIMULUS RESPONSE;

EID: 84925114382     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2015.00054     Document Type: Article

References (57)

1. Anselme, P., Robinson, M. J., and Berridge, K. C. (2013). Reward uncertainty enhances incentive salience attribution as sign-tracking. Behav. Brain Res. 238, 53-61. doi: 10.1016/j.bbr.2012.10.006.
2. Atnip, G. W. (1977). Stimulus- and response-reinforcer contingencies in autoshaping, operant, classical, and omission training procedures in rats. J. Exp. Anal. Behav. 28, 59-69. doi: 10.1901/jeab.1977.28-59.
3. Attwood, A. S., Scott-Samuel, N. E., Stothart, G., and Munafo, M. R. (2012). Glass shape influences consumption rate for alcoholic beverages. PLoS ONE 7:e43007. doi: 10.1371/journal.pone.0043007.
4. Back, S. E., Gros, D. F., Mccauley, J. L., Flanagan, J. C., Cox, E., Barth, K. S., et al. (2014). Laboratory-induced cue reactivity among individuals with prescription opioid dependence. Addict. Behav. 39, 1217-1223. doi: 10.1016/j.addbeh.2014.04.007.
5. Berridge, K. C., and Robinson, T. E. (1998). What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain research. Brain Res. Rev. 28, 309-369. doi: 10.1016/S0165-0173(98)00019-8.
6. Bindra, D. (1974). A motivational view of learning, performance, and behavior modification. Psychol. Rev. 81, 199-213. doi: 10.1037/h0036330.
7. Caggiula, A. R., Donny, E. C., White, A. R., Chaudhri, N., Booth, S., Gharib, M. A., et al. (2001). Cue dependency of nicotine self-administration and smoking. Pharmacol. Biochem. Behav. 70, 515-530. doi: 10.1016/S0091-3057(01)00676-1.
8. Carrillo, J., Howard, E. C., Moten, M., Houck, B. D., Czachowski, C. L., and Gonzales, R. A. (2008). A 3-day exposure to 10% ethanol with 10% sucrose successfully initiates ethanol self-administration. Alcohol 42, 171-178. doi: 10.1016/j.alcohol.2008.01.005.
9. Chaudhri, N., Caggiula, A. R., Donny, E. C., Booth, S., Gharib, M., Craven, L., et al. (2006). Operant responding for conditioned and unconditioned reinforcers in rats is differentially enhanced by the primary reinforcing and reinforcement-enhancing effects of nicotine. Psychopharmacology 189, 27-36. doi: 10.1007/s00213-006-0522-0.
10. Chaudhri, N., Caggiula, A. R., Donny, E. C., Booth, S., Gharib, M., Craven, L., et al. (2007). Self-administered and noncontingent nicotine enhance reinforced operant responding in rats: impact of nicotine dose and reinforcement schedule. Psychopharmacology 190, 353-362. doi: 10.1007/s00213-006-0454-8.
11. Chaudhri, N., Sahuque, L. L., and Janak, P. H. (2008). Context-induced relapse of conditioned behavioral responding to ethanol cues in rats. Biol. Psychiatry 64, 203-210. doi: 10.1016/j.biopsych.2008.03.007.
12. Childress, A. R., Mozley, P. D., Mcelgin, W., Fitzgerald, J., Reivich, M., and O'brien, C. P. (1999). Limbic activation during cue-induced cocaine craving. Am. J. Psychiatry 156, 11-18. doi: 10.1176/ajp.156.1.11.
13. De Wit, H., and Stewart, J. (1981). Reinstatement of cocaine-reinforced responding in the rat. Psychopharmacology75, 134-143. doi: 10.1007/BF00432175.
14. Di Ciano, P., and Everitt, B. J. (2004). Conditioned reinforcing properties of stimuli paired with self-administered cocaine, heroin or sucrose: implications for the persistence of addictive behaviour. Neuropharmacology 47(Suppl. 1), 202-213. doi: 10.1016/j.neuropharm.2004.06.005.
15. Difeliceantonio, A. G., and Berridge, K. C. (2012). Which cue to 'want'? Opioid stimulation of central amygdala makes goal-trackers show stronger goal-tracking, just as sign-trackers show stronger sign-tracking. Behav. Brain Res. 230, 399-408. doi: 10.1016/j.bbr.2012.02.032.
16. Fedorchak, P. M., and Bolles, R. C. (1987). Hunger enhances the expression of calorie- but not taste-mediated conditioned flavor preferences. J. Exp. Psychol. Anim. Behav. Process. 13, 73-79. doi: 10.1037/0097-7403.13.1.73.
17. Field, M., and Cox, W. M. (2008). Attentional bias in addictive behaviors: a review of its development, causes, and consequences. Drug Alcohol Depend. 97, 1-20. doi: 10.1016/j.drugalcdep.2008.03.030.
18. Field, M., and Duka, T. (2002). Cues paired with a low dose of alcohol acquire conditioned incentive properties in social drinkers. Psychopharmacology 159, 325-334. doi: 10.1007/s00213-001-0923-z.
19. Flagel, S. B., Akil, H., and Robinson, T. E. (2009). Individual differences in the attribution of incentive salience to reward-related cues: implications for addiction. Neuropharmacology 56(Suppl. 1), 139-148. doi: 10.1016/j.neuropharm.2008.06.027.
20. Flagel, S. B., Cameron, C. M., Pickup, K. N., Watson, S. J., Akil, H., and Robinson, T. E. (2011a). A food predictive cue must be attributed with incentive salience for it to induce c-fos mRNA expression in cortico-striatal-thalamic brain regions. Neuroscience 196, 80-96. doi: 10.1016/j.neuroscience.2011.09.004.
21. Flagel, S. B., Clark, J. J., Robinson, T. E., Mayo, L., Czuj, A., Willuhn, I., et al. (2011b). A selective role for dopamine in stimulus-reward learning. Nature 469, 53-57. doi: 10.1038/nature09588.
22. Fletcher, P. J., Korth, K. M., Robinson, S. R., and Baker, G. B. (2002). Multiple 5-HT receptors are involved in the effects of acute MDMA treatment: studies on locomotor activity and responding for conditioned reinforcement.Psychopharmacology 162, 282-291. doi: 10.1007/s00213-002-1104-4.
23. Grimm, J. W., Hope, B. T., Wise, R. A., and Shaham, Y. (2001). Neuroadaptation. Incubation of cocaine craving after withdrawal. Nature 412, 141-142. doi: 10.1038/35084134.
24. Guy, E. G., and Fletcher, P. J. (2013). Nicotine-induced enhancement of responding for conditioned reinforcement in rats: role of prior nicotine exposure and alpha4beta2 nicotinic receptors. Psychopharmacology 225, 429-440. doi: 10.1007/s00213-012-2832-8.
25. Hogarth, L., Dickinson, A., and Duka, T. (2003). Discriminative stimuli that control instrumental tobacco-seeking by human smokers also command selective attention. Psychopharmacology 168, 435-445. doi: 10.1007/s00213-003-1456-4.
26. Krank, M. D. (2003). Pavlovian conditioning with ethanol: sign-tracking (autoshaping), conditioned incentive, and ethanol self-administration. Alcohol. Clin. Exp. Res. 27, 1592-1598. doi: 10.1097/01.ALC.0000092060.09228.DE.
27. Krank, M. D., O'neill, S., Squarey, K., and Jacob, J. (2008). Goal- and signal-directed incentive: conditioned approach, seeking, and consumption established with unsweetened alcohol in rats. Psychopharmacology 196, 397-405. doi: 10.1007/s00213-007-0971-0.
28. Lesaint, F., Sigaud, O., Flagel, S. B., Robinson, T. E., and Khamassi, M. (2014). Modelling individual differences in the form of pavlovian conditioned approach responses: a dual learning systems approach with factored representations. PLoS Comput. Biol. 10:e1003466. doi: 10.1371/journal.pcbi.1003466.
29. Litt, M. D., and Cooney, N. L. (1999). Inducing craving for alcohol in the laboratory. Alcohol Res. Health 23, 174-178.
30. Litt, M. D., Cooney, N. L., and Morse, P. (2000). Reactivity to alcohol-related stimuli in the laboratory and in the field: predictors of craving in treated alcoholics. Addiction 95, 889-900. doi: 10.1046/j.1360-0443.2000.9568896.x.
31. Lockie, S. H., and Andrews, Z. B. (2013). The hormonal signature of energy deficit: Increasing the value of food reward. Mol. Metab. 2, 329-336. doi: 10.1016/j.molmet.2013.08.003.
32. Lof, E., Olausson, P., Stomberg, R., Taylor, J. R., and Soderpalm, B. (2010). Nicotinic acetylcholine receptors are required for the conditioned reinforcing properties of sucrose-associated cues. Psychopharmacology 212, 321-328. doi: 10.1007/s00213-010-1957-x.
33. Meyer, P. J., Cogan, E. S., and Robinson, T. E. (2014). The form of a conditioned stimulus can influence the degree to which it acquires incentive motivational properties. PLoS ONE 9:e98163. doi: 10.1371/journal.pone.0098163.
34. Meyer, P. J., Lovic, V., Saunders, B. T., Yager, L. M., Flagel, S. B., Morrow, J. D., et al. (2012a). Quantifying individual variation in the propensity to attribute incentive salience to reward cues. PLoS ONE 7:e38987. doi: 10.1371/journal.pone.0038987.
35. Meyer, P. J., Ma, S. T., and Robinson, T. E. (2012b). A cocaine cue is more preferred and evokes more frequency-modulated 50-kHz ultrasonic vocalizations in rats prone to attribute incentive salience to a food cue.Psychopharmacology 219, 999-1009. doi: 10.1007/s00213-011-2429-7.
36. Morrow, J. D., Saunders, B. T., Maren, S., and Robinson, T. E. (2015). Sign-tracking to an appetitive cue predicts incubation of conditioned fear in rats. Behav. Brain Res. 276, 59-66. doi: 10.1016/j.bbr.2014.04.002.
37. O'Connell, M. F. (1979). Temporal distributions of responding during discrete-trial omission training in rats. J. Exp. Anal. Behav. 31, 31-40. doi: 10.1901/jeab.1979.31-31.
38. Olausson, P., Jentsch, J. D., and Taylor, J. R. (2004). Nicotine enhances responding with conditioned reinforcement. Psychopharmacology 171, 173-178. doi: 10.1007/s00213-003-1575-y.
39. Peters, J., and De Vries, T. J. (2014). Pavlovian conditioned approach, extinction, and spontaneous recovery to an audiovisual cue paired with an intravenous heroin infusion. Psychopharmacology 231, 447-453. doi: 10.1007/s00213-013-3258-7.
40. Ramirez, J., and Miranda, R. Jr. (2014). Alcohol craving in adolescents: bridging the laboratory and natural environment. Psychopharmacology 231, 1841-1851. doi: 10.1007/s00213-013-3372-6.
41. Robinson, T. E., and Berridge, K. C. (1993). The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain research. Brain Res. Rev. 18, 247-291. doi: 10.1016/0165-0173(93)90013-P.
42. Robinson, T. E., and Flagel, S. B. (2009). Dissociating the predictive and incentive motivational properties of reward-related cues through the study of individual differences. Biol. Psychiatry 65, 869-873. doi: 10.1016/j.biopsych.2008.09.006.
43. Samson, H. H., Roehrs, T. A., and Tolliver, G. A. (1982). Ethanol reinforced responding in the rat: a concurrent analysis using sucrose as the alternate choice. Pharmacol. Biochem. Behav. 17, 333-339. doi: 10.1016/0091-3057(82)90088-0.
44. Sanabria, F., Sitomer, M. T., and Killeen, P. R. (2006). Negative automaintenance omission training is effective. J. Exp. Anal. Behav. 86, 1-10. doi: 10.1901/jeab.2006.36-05.
45. Saunders, B. T., and Robinson, T. E. (2012). The role of dopamine in the accumbens core in the expression of Pavlovian-conditioned responses. Eur. J. Neurosci. 36, 2521-2532. doi: 10.1111/j.1460-9568.2012.08217.x.
46. Simms, J. A., Steensland, P., Medina, B., Abernathy, K. E., Chandler, L. J., Wise, R., et al. (2008). Intermittent access to 20% ethanol induces high ethanol consumption in Long-Evans and Wistar rats. Alcohol. Clin. Exp. Res. 32, 1816-1823. doi: 10.1111/j.1530-0277.2008.00753.x.
47. Sinha, R., and O'Malley, S. S. (1999). Craving for alcohol: findings from the clinic and the laboratory. Alcohol Alcohol. 34, 223-230. doi: 10.1093/alcalc/34.2.223.
48. Smith, S. G., Werner, T. E., and Davis, W. M. (1977). Alcohol-associated conditioned reinforcement.Psychopharmacology 53, 223-226. doi: 10.1007/BF00492355.
49. Sparks, L. M., Sciascia, J. M., Ayorech, Z., and Chaudhri, N. (2013). Vendor differences in alcohol consumption and the contribution of dopamine receptors to Pavlovian-conditioned alcohol-seeking in Long-Evans rats.Psychopharmacology 231, 753-764. doi: 10.1007/s00213-013-3292-5.
50. Stiers, M., and Silberberg, A. (1974). Lever-contact responses in rats: automaintenance with and without a negative response-reinforcer dependency. J. Exp. Anal. Behav. 22, 497-506. doi: 10.1901/jeab.1974.22-497.
51. Tomie, A., Di Poce, J., Derenzo, C. C., and Pohorecky, L. A. (2002). Autoshaping of ethanol drinking: an animal model of binge drinking. Alcohol Alcohol. 37, 138-146. doi: 10.1093/alcalc/37.2.138.
52. Tomie, A., Festa, E. D., Sparta, D. R., and Pohorecky, L. A. (2003). Lever conditioned stimulus-directed autoshaping induced by saccharin-ethanol unconditioned stimulus solution: effects of ethanol concentration and trial spacing. Alcohol 30, 35-44. doi: 10.1016/S0741-8329(03)00069-7.
53. Uslaner, J. M., Acerbo, M. J., Jones, S. A., and Robinson, T. E. (2006). The attribution of incentive salience to a stimulus that signals an intravenous injection of cocaine. Behav. Brain Res. 169, 320-324. doi: 10.1016/j.bbr.2006.02.001.
54. Williams, D. R., and Williams, H. (1969). Auto-maintenance in the pigeon: sustained pecking despite contingent non-reinforcement. J. Exp. Anal. Behav. 12, 511-520. doi: 10.1901/jeab.1969.12-511.
55. Wise, R. A. (1973). Voluntary ethanol intake in rats following exposure to ethanol on various schedules.Psychopharmacologia 29, 203-210. doi: 10.1007/BF00414034.
56. Yager, L. M., and Robinson, T. E. (2010). Cue-induced reinstatement of food seeking in rats that differ in their propensity to attribute incentive salience to food cues. Behav. Brain Res. 214, 30-34. doi: 10.1016/j.bbr.2010.04.021.
57. Yager, L. M., and Robinson, T. E. (2013). A classically conditioned cocaine cue acquires greater control over motivated behavior in rats prone to attribute incentive salience to a food cue. Psychopharmacology 226, 217-228. doi: 10.1007/s00213-012-2890-y.