[en] Uncertainty is a component of many gambling games and may play a role in incentive motivation and cue attraction. Uncertainty can increase the attractiveness for predictors of reward in the Pavlovian procedure of autoshaping, visible as enhanced sign-tracking (or approach and nibbles) by rats of a metal lever whose sudden appearance acts as a conditioned stimulus (CS+) to predict sucrose pellets as an unconditioned stimulus (UCS). Here we examined how reward uncertainty might enhance incentive salience as sign-tracking both in intensity and by broadening the range of attractive CS+s. We also examined whether initially-induced uncertainty enhancements of CS+ attraction can endure beyond uncertainty itself, and persist even when Pavlovian prediction becomes 100% certain. Our results show that uncertainty can broaden incentive salience attribution to make CS cues attractive that would otherwise not be (either because they are too distal from reward or too risky to normally attract sign-tracking). In addition, uncertainty enhancement of CS+ incentive salience, once induced by initial exposure, persisted even when Pavlovian CS-UCS correlations later rose toward 100% certainty in prediction. Persistence suggests an enduring incentive motivation enhancement potentially relevant to gambling, which in some ways resembles incentive-sensitization. Higher motivation to uncertain CS+s leads to more potent attraction to these cues when they predict the delivery of uncertain rewards. In humans, those cues might possibly include the sights and sounds associated with gambling, which contribute a major component of the play immersion experienced by problematic gamblers.
Disciplines :
Neurosciences & behavior
Author, co-author :
Robinson, Mike J.F.
Anselme, Patrick ; Université de Liège - ULiège > Département de Psychologie : cognition et comportement > Neuroscience comportementale et psychopharmacologie expér.
Fischer, Adam M.
Berridge, Kent C.
Language :
English
Title :
Initial uncertainty in Pavlovian reward prediction persistently elevates incentive salience and extends sign-tracking to normally unattractive cues
Dow Schüll N. Addiction by design: machine gambling in Las Vegas 2012, Princeton University Press, Princeton, NJ. First edition.
Costikyan G. Uncertainty in games 2013, MIT Press, Cambridge, MA.
Ashrafioun L., McCarthy A., Rosenberg H. Assessing the impact of cue exposure on craving to gamble in university students. J Gambl Stud 2012, 28:363-375.
Boakes R.A. Performance on learning to associate a stimulus with positive reinforcement. Operant Pavlovian interactions 1977, vol. Book Chapter:67-97. Erlbaum Associates, Hillsdale, NJ.
Flagel S.B., Watson S.J., Robinson T.E., Akil H. Individual differences in the propensity to approach signals vs goals promote different adaptations in the dopamine system of rats. Psychopharmacology (Berl) 2007, 191:599-607.
Flagel S.B., Clark J.J., Robinson T.E., Mayo L., Czuj A., Willuhn I., et al. A selective role for dopamine in stimulus-reward learning. Nature 2011, 469:53-57.
Meyer P.J., Lovic V., Saunders B.T., Yager L.M., Flagel S.B., Morrow J.D., et al. Quantifying individual variation in the propensity to attribute incentive salience to reward cues. PLoS ONE 2012, 7:e38987.
Robinson T.E., Flagel S.B. Dissociating the predictive and incentive motivational properties of reward-related cues through the study of individual differences. Biol Psychiatry 2009, 65:869-873.
Saunders B.T., Robinson T.E. The role of dopamine in the accumbens core in the expression of Pavlovian-conditioned responses. Eur J Neurosci 2012, 36:2521-2532.
Tomie A. Locating reward cue at response manipulandum (CAM) induces symptoms of drug abuse. Neurosci Biobehav Rev 1996, 20:505-535.
Rescorla R.A., Wagner A.R. A theory of pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. Classical conditioning II: current theory and research 1972, 64-99. Appleton-Century-Crofts, New York. A.H. Black, W.F. Prokasy (Eds.).
Schultz W. Predictive reward signal of dopamine neurons. J Neurophysiol 1998, 80:1-27.
van Duuren E., van der Plasse G., Lankelma J., Joosten R.N.J.M.A., Feenstra M.G.P., Pennartz C.M.A. Single-cell and population coding of expected reward probability in the orbitofrontal cortex of the rat. J Neurosci 2009, 29:8965-8976.
Smith K.S., Berridge K.C., Aldridge J.W. Disentangling pleasure from incentive salience and learning signals in brain reward circuitry. Proc Natl Acad Sci USA 2011, 108:E255-E264.
Robinson M.J.F., Berridge K.C. Instant transformation of learned repulsion into motivational "wanting". Curr Biol 2013, 23:282-289.
Davison M.C. Preference for mixed-interval versus fixed-interval schedules. J Exp Anal Behav 1969, 12:247-252.
Collins L., Young D.B., Davies K., Pearce J.M. The influence of partial reinforcement on serial autoshaping with pigeons. Q J Exp Psychol B 1983, 35:275-290.
Forkman B.A. The effect of uncertainty on the food intake of the Mongolian Gerbil. Behaviour 1993, 124:197-206.
Hurly T., Oseen M. Context-dependent, risk-sensitive foraging preferences in wild rufous hummingbirds. Animal Behaviour 1999, 58:59-66.
Adriani W., Laviola G. Delay aversion but preference for large and rare rewards in two choice tasks: implications for the measurement of self-control parameters. BMC Neurosci 2006, 7:52.
Molet M., Miller H.C., Laude J.R., Kirk C., Manning B., Zentall T.R. Decision making by humans in a behavioral task: do humans, like pigeons, show suboptimal choice?. Learn Behav 2012, 40:439-447.
Anselme P., Robinson M.J.F., Berridge K.C. Reward uncertainty enhances incentive salience attribution as sign-tracking. Behav Brain Res 2013, 238:53-61.
St Onge J.R., Stopper C.M., Zahm D.S., Floresco S.B. Separate prefrontal-subcortical circuits mediate different components of risk-based decision making. J Neurosci 2012, 32:2886-2899.
Linnet J., Mouridsen K., Peterson E., Møller A., Doudet D.J., Gjedde A. Striatal dopamine release codes uncertainty in pathological gambling. Psychiatry Res 2012, 204:55-60.
Joutsa J., Johansson J., Niemelä S., Ollikainen A., Hirvonen M.M., Piepponen P., et al. Mesolimbic dopamine release is linked to symptom severity in pathological gambling. Neuroimage 2012, 60:1992-1999.
Linnet J. The Iowa gambling task and the three fallacies of dopamine in gambling disorder. Front Psychol 2013, 4:709.
Silva F.J., Silva K.M., Pear J.J. Sign- versus goal-tracking: effects of conditioned-stimulus-to-unconditioned-stimulus distance. J Exp Anal Behav 1992, 57:17-31.
Haller J., Alicki M. Current animal models of anxiety, anxiety disorders, and anxiolytic drugs. Curr Opin Psychiatry 2012, 25:59-64.
Scherrer J.F., Xian H., Kapp J.M.K., Waterman B., Shah K.R., Volberg R., et al. Association between exposure to childhood and lifetime traumatic events and lifetime pathological gambling in a twin cohort. J Nerv Ment Dis 2007, 195:72-78.
Braverman J., Shaffer H.J. How do gamblers start gambling: identifying behavioural markers for high-risk internet gambling. Eur J Public Health 2012, 22:273-278.
Lomanowska A.M., Lovic V., Rankine M.J., Mooney S.J., Robinson T.E., Kraemer G.W. Inadequate early social experience increases the incentive salience of reward-related cues in adulthood. Behav Brain Res 2011, 220:91-99.
Robinson T.E., Berridge K.C. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev 1993, 18:247-291.
Fiorillo C.D., Tobler P.N., Schultz W. Discrete coding of reward probability and uncertainty by dopamine neurons. Science 2003, 299:1898-1902.
Fiorillo C.D. Transient activation of midbrain dopamine neurons by reward risk. Neuroscience 2011, 197:162-171.
Singer B.F., Scott-Railton J., Vezina P. Unpredictable saccharin reinforcement enhances locomotor responding to amphetamine. Behav Brain Res 2012, 226:340-344.
Piazza P.V., Deminiere J.M., le Moal M., Simon H. Stress- and pharmacologically-induced behavioral sensitization increases vulnerability to acquisition of amphetamine self-administration. Brain Res 1990, 514:22-26.
Tomie A., Tirado A.D., Yu L., Pohorecky L.A. Pavlovian autoshaping procedures increase plasma corticosterone and levels of norepinephrine and serotonin in prefrontal cortex in rats. Behav Brain Res 2004, 153:97-105.
Flagel S.B., Akil H., Robinson T.E. Individual differences in the attribution of incentive salience to reward-related cues: implications for addiction. Neuropharmacology 2009, 56(Suppl 1):139-148.
Flagel S.B., Cameron C.M., Pickup K.N., Watson S.J., Akil H., Robinson T.E. 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 2011, 196:80-96.
Berridge K.C., Robinson T.E. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?. Brain Res Brain Res Rev 1998, 28:309-369.
Berridge K.C. The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology (Berl) 2007, 191:391-431.
Saunders B.T., Yager L.M., Robinson T.E. Cue-evoked cocaine "craving": role of dopamine in the accumbens core. J Neurosci 2013, 33:13989-14000.
de Lafuente V., Romo R. Dopamine neurons code subjective sensory experience and uncertainty of perceptual decisions. Proc Natl Acad Sci USA 2011, 108:19767-19771.
Aron A.R., Shohamy D., Clark J., Myers C., Gluck M.A., Poldrack R.A. Human midbrain sensitivity to cognitive feedback and uncertainty during classification learning. J Neurophysiol 2004, 92:1144-1152.
Preuschoff K., Bossaerts P., Quartz S.R. Neural differentiation of expected reward and risk in human subcortical structures. Neuron 2006, 51:381-390.
Monosov I.E., Hikosaka O. Selective and graded coding of reward uncertainty by neurons in the primate anterodorsal septal region. Nat Neurosci 2013, 16:756-762.
