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Individual Differences in the Attribution of Incentive Salience to a Pavlovian Alcohol Cue


Individual Differences in the Attribution of Incentive Salience to a Pavlovian Alcohol Cue

Villaruel, Franz R. and Chaudhri, Nadia ORCID: https://orcid.org/0000-0003-4217-4044 (2016) Individual Differences in the Attribution of Incentive Salience to a Pavlovian Alcohol Cue. Frontiers in Behavioral Neuroscience, 10 (238). ISSN 1662-5153

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Official URL: http://dx.doi.org/10.3389/fnbeh.2016.00238


Individual differences exist in the attribution of incentive salience to conditioned stimuli associated with food. Here, we investigated whether individual differences also manifested with a Pavlovian alcohol conditioned stimulus (CS). We compiled data from five experiments that used a Pavlovian autoshaping paradigm and tests of conditioned reinforcement. In all experiments, male, Long-Evans rats with unrestricted access to food and water were acclimated to 15% ethanol. Next, rats received Pavlovian autoshaping training, in which a 10 s presentation of a retractable lever served as the CS and 0.2 mL of 15% ethanol served as the unconditioned stimulus (US). Finally, rats underwent conditioned reinforcement tests in which nose-pokes to an active aperture led to brief presentations of the lever-CS, but nose-pokes to an inactive aperture had no consequence. Rats were categorized as sign-trackers, goal-trackers and intermediates based on a response bias score that reflected their tendencies to sign-track or goal-track at different times during training. We found that distinct groups of rats either consistently interacted with the lever-CS (“sign-trackers”) or routinely approached the port during the lever-CS (“goal-trackers”) across a majority of the training sessions. However, some individuals (“shifted sign-trackers”) with an early tendency to goal-track later shifted to comparable asymptotic levels of sign-tracking as the group identified as sign-trackers. The lever-CS functioned as a conditioned reinforcer for sign-trackers and shifted sign-trackers, but not for goal-trackers. These results provide evidence of robust individual differences in the extent to which a Pavlovian alcohol cue gains incentive salience and functions as a conditioned reinforcer.

Divisions:Concordia University > Faculty of Arts and Science > Psychology
Item Type:Article
Authors:Villaruel, Franz R. and Chaudhri, Nadia
Journal or Publication:Frontiers in Behavioral Neuroscience
Date:26 December 2016
  • Canadian Institutes of Health Research (CIHR)
  • Concordia Open Access Author Fund
Digital Object Identifier (DOI):10.3389/fnbeh.2016.00238
Keywords:sign-tracking, goal-tracking, incentive salience, autoshaping, conditioned reinforcement, Pavlovian conditioning, alcohol, individual differences
ID Code:982641
Deposited By: Danielle Dennie
Deposited On:21 Jun 2017 15:42
Last Modified:18 Jan 2018 17:55


Abrahao, K. P., Quadros, I. M. H., and Souza-Formigoni, M. L. O. (2011). Nucleus accumbens dopamine D1 receptors regulate the expression of ethanol-induced behavioural sensitization. Int. J. Neuropsychopharmacol. 14, 175–185. doi: 10.1017/s1461145710000441

Anselme, P., Robinson, M. J. F., 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

Boakes, R. (1977). “Performance on learning to associate a stimulus with positive reinforcement,” in Operant-Pavlovian Interactions, eds H. Davis and H. Hurwitz (Hillsdale, NJ: Lawrence Erlbaum Associates), 67–97.

Brodie, M. S. (2002). Increased ethanol excitation of dopaminergic neurons of the ventral tegmental area after chronic ethanol treatment. Alcohol. Clin. Exp. Res. 26, 1024–1030. doi: 10.1097/00000374-200207000-00013

Brown, P. L., and Jenkins, H. M. (1968). Auto-shaping of the pigeon’s key-peck. J. Exp. Anal. Behav. 11, 1–8. doi: 10.1901/jeab.1968.11-1

Cardinal, R. N., Parkinson, J. A., Hall, J., and Everitt, B. J. (2002). Emotion and motivation: the role of the amygdala, ventral striatum and prefrontal cortex. Neurosci. Biobehav. Rev. 26, 321–352. doi: 10.1016/s0149-7634(02)00007-6

Carnicella, S., Ron, D., and Barak, S. (2014). Intermittent ethanol access schedule in rats as a preclinical model of alcohol abuse. Alcohol 48, 243–252. doi: 10.1016/j.alcohol.2014.01.006

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

Dalley, J. W., Lääne, K., Theobald, D. E. H., Armstrong, H. C., Corlett, P. R., Chudasama, Y., et al. (2005). Time-limited modulation of appetitive Pavlovian memory by D1 and NMDA receptors in the nucleus accumbens. Proc. Natl. Acad. Sci. U S A 102, 6189–6194. doi: 10.1073/pnas.0502080102

Davey, G. C., and Cleland, G. G. (1982). Topography of signal-centered behavior in the rat: effects of deprivation state and reinforcer type. J. Exp. Anal. Behav. 38, 291–304. doi: 10.1901/jeab.1982.38-291

Doremus-Fitzwater, T. L., and Spear, L. P. (2011). Amphetamine-induced incentive sensitization of sign-tracking behavior in adolescent and adult female rats. Behav. Neurosci. 125, 661–667. doi: 10.1037/a0023763

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, 139–148. doi: 10.1016/j.neuropharm.2008.06.027

Flagel, S. B., Watson, S. J., Akil, H., and Robinson, T. E. (2008). Individual differences in the attribution of incentive salience to a reward-related cue: influence on cocaine sensitization. Behav. Brain Res. 186, 48–56. doi: 10.1016/j.bbr.2007.07.022

Flagel, S. B., Watson, S. J., Robinson, T. E., and Akil, H. (2007). Individual differences in the propensity to approach signals vs. goals promote different adaptations in the dopamine system of rats. Psychopharmacology 191, 599–607. doi: 10.1007/s00213-006-0535-8

Guy, E. G., and Fletcher, P. J. (2013). Nicotine-induced enhancement of responding for conditioned reinforcement in rats: role of prior nicotine exposure and α4β2 nicotinic receptors. Psychopharmacology 225, 429–440. doi: 10.1007/s00213-012-2832-8

Hearst, E., and Jenkins, H. M. (1974). Sign Tracking: The Stimulus-reinforcer Relation and Directed Action. Austin: Monograph of the Psychonomic Society.

Kawa, A. B., Bentzley, B. S., and Robinson, T. E. (2016). Less is more: prolonged intermittent access cocaine self-administration produces incentive-sensitization and addiction-like behavior. Psychopharmacology 233, 3587–3602. doi: 10.1007/s00213-016-4393-8

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

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

Löf, E., Olausson, P., Stomberg, R., Taylor, J. R., and Söderpalm, 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

Lomanowska, A. M., Lovic, V., Rankine, M. J., Mooney, S. J., Robinson, T. E., and Kraemer, G. W. (2011). Inadequate early social experience increases the incentive salience of reward-related cues in adulthood. Behav. Brain Res. 220, 91–99. doi: 10.1016/j.bbr.2011.01.033

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

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

Milton, A. L., and Everitt, B. J. (2010). The psychological and neurochemical mechanisms of drug memory reconsolidation: implications for the treatment of addiction. Eur. J. Neurosci. 31, 2308–2319. doi: 10.1111/j.1460-9568.2010.07249.x

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

Palmatier, M. I., Marks, K. R., Jones, S. A., Freeman, K. S., Wissman, K. M., and Sheppard, A. B. (2013). The effect of nicotine on sign-tracking and goal-tracking in a Pavlovian conditioned approach paradigm in rats. Psychopharmacology 226, 247–259. doi: 10.1007/s00213-012-2892-9

Robinson, M. J. F., Anselme, P., Suchomel, K., and Berridge, K. C. (2015). Amphetamine-induced sensitization and reward uncertainty similarly enhance incentive salience for conditioned cues. Behav. Neurosci. 129, 502–511. doi: 10.1037/bne0000064

Robinson, T. E., and Berridge, K. C. (1993). The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res. Rev. 18, 247–291. doi: 10.1016/0165-0173(93)90013-p

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

Saunders, B. T., O’Donnell, E. G., Aurbach, E. L., and Robinson, T. E. (2014). A cocaine context renews drug seeking preferentially in a subset of individuals. Neuropsychopharmacology 39, 2816–2823. doi: 10.1038/npp.2014.131

Saunders, B. T., and Robinson, T. E. (2010). A cocaine cue acts as an incentive stimulus in some but not others: implications for addiction. Biol. Psychiatry 67, 730–736. doi: 10.1016/j.biopsych.2009.11.015

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

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

Srey, C. S., Maddux, J-M. N., and Chaudhri, N. (2015). The attribution of incentive salience to Pavlovian alcohol cues: a shift from goal-tracking to sign-tracking. Front. Behav. Neurosci. 9:54. doi: 10.3389/fnbeh.2015.00054

Stewart, J., de Wit, H., and Eikelboom, R. (1984). Role of unconditioned and conditioned drug effects in the self-administration of opiates and stimulants. Psychol. Rev. 91, 251–268. doi: 10.1037//0033-295x.91.2.251

Tomie, A., Aguado, A. S., Pohorecky, L. A., and Benjamin, D. (2000). Individual differences in pavlovian autoshaping of lever pressing in rats predict stress-induced corticosterone release and mesolimbic levels of monoamines. Pharmacol. Biochem. Behav. 65, 509–517. doi: 10.1016/s0091-3057(99)00241-5

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

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

Wise, R. A. (1973). Voluntary ethanol intake in rats following exposure to ethanol on various schedules. Psychopharmacologia 29, 203–210. doi: 10.1007/bf00414034

Yager, L. M., Pitchers, K. K., Flagel, S. B., and Robinson, T. E. (2015). Individual variation in the motivational and neurobiological effects of an opioid cue. Neuropsychopharmacology 40, 1269–1277. doi: 10.1038/npp.2014.314

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
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