Sign tracking, but not goal tracking, is resistant to outcome devaluation

Frontiers in Neuroscience

Volumn 9, Issue DEC, 2015, Pages

  Morrison, Sara E ^a,b   Bamkole, Michael A ^a   Nicola, Saleem M ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Devaluation; Goal tracking; Pavlovian conditioning; Rats; Reward; Sign tracking

Indexed keywords

SUCROSE;

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONDITIONED STIMULUS; CONDITIONING; CONTROLLED STUDY; EXPERIMENTAL BEHAVIORAL TEST; GOAL TRACKING; MALE; NONHUMAN; PAVLOVIAN CONDITIONING; RAT; REWARD; REWARD DEVALUATION; SIGN TRACKING BEHAVIOR;

EID: 84954523756     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2015.00468     Document Type: Article

References (46)

1. Ahrens, A. M., Singer, B. F., Fitzpatrick, C. J., Morrow, J. D., and Robinson, T. E. (2015). Rats that sign-track are resistant to Pavlovian but not instrumental extinction. Behav. Brain Res. 296, 418-430. doi: 10.1016/j.bbr.2015.07.055.
2. Ambroggi, F., Ghazizadeh, A., Nicola, S. M., and Fields, H. L. (2011). Roles of nucleus accumbens core and shell in incentive-cue responding and behavioral inhibition. J. Neurosci. 31, 6820-6830. doi: 10.1523/JNEUROSCI.6491-10.2011.
3. Ambroggi, F., Ishikawa, A., Fields, H. L., and Nicola, S. M. (2008). Basolateral amygdala neurons facilitate reward-seeking behavior by exciting nucleus accumbens neurons. Neuron 59, 648-661. doi: 10.1016/j.neuron.2008.07.004.
4. 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.
5. Beckmann, J. S., and Chow, J. J. (2015). Isolating the incentive salience of reward-associated stimuli: value, choice, and persistence. Learn. Mem. 22, 116-127. doi: 10.1101/lm.037382.114.
6. Berridge, K. C. (2004). Motivation concepts in behavioral neuroscience. Physiol. Behav. 81, 179-209. doi: 10.1016/j.physbeh.2004.02.004.
7. 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.
8. Boakes, R. A. (1977). "Performance on learning to associate a stimulus with positive reinforcement," in Operant-Pavlovian Interactions, eds H. Davis and H. M. B. Hurwitz (Hillsdale, NJ: Lawrence Erlbaum Associates), 67-97.
9. Chang, S. E., and Holland, P. C. (2013). Effects of nucleus accumbens core and shell lesions on autoshaped lever-pressing. Behav. Brain Res. 256, 36-42. doi: 10.1016/j.bbr.2013.07.046.
10. Clark, J. J., Hollon, N. G., and Phillips, P. E. (2012). Pavlovian valuation systems in learning and decision making. Curr. Opin. Neurobiol. 22, 1054-1061. doi: 10.1016/j.conb.2012.06.004.
11. Cleland, G. G., and Davey, G. C. (1982). The effects of satiation and reinforcer devaluation on signal-centered behavior in the rat. Learn. Motiv. 13, 343-360.
12. 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.
13. Derman, R., and Delamater, A. R. (2014). "Conditioned sign tracking in rats is mediated by a representation of the goal," in Society for Neuroscience Abstracts (Washington, DC: Society for Neuroscience).
14. Di Ciano, P., Cardinal, R. N., Cowell, R. A., Little, S. J., and Everitt, B. J. (2001). 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, 9471-9477.
15. du Hoffmann, J., and Nicola, S. M. (2014). Dopamine invigorates reward seeking by promoting cue-evoked excitation in the nucleus accumbens. J. Neurosci. 34, 14349-14364. doi: 10.1523/JNEUROSCI.3492-14.2014.
16. Everitt, B. J., and Robbins, T. W. (2005). Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat. Neurosci. 8, 1481-1489. doi: 10.1038/nn1579.
17. Fitzpatrick, C. J., Gopalakrishnan, S., Cogan, E. S., Yager, L. M., Meyer, P. J., Lovic, V., et al. (2013). Variation in the form of Pavlovian conditioned approach behavior among outbred male Sprague-Dawley rats from different vendors and colonies: sign-tracking vs. goal-tracking. PLoS ONE 8:e75042. doi: 10.1371/journal.pone.0075042.
18. 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.
19. 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.
20. 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.
21. Flagel, S. B., Robinson, T. E., Clark, J. J., Clinton, S. M., Watson, S. J., Seeman, P., et al. (2010). An animal model of genetic vulnerability to behavioral disinhibition and responsiveness to reward-related cues: implications for addiction. Neuropsychopharmacology 35, 388-400. doi: 10.1038/npp.2009.142.
22. Gallagher, M., Mcmahan, R. W., and Schoenbaum, G. (1999). Orbitofrontal cortex and representation of incentive value in associative learning. J. Neurosci. 19, 6610-6614.
23. Hearst, E., and Jenkins, H. M. (1974). Sign-tracking: The Stimulus-reinforcer Relation and Directed Action. Austin, TX: Psychonomic Society.
24. Hilliard, S., and Domjan, M. (1995). Effects of sexual conditioning of devaluing the US through satiation. Q. J. Exp. Psychol. B 48, 84-92.
25. Holloway, K. S., and Domjan, M. (1993). Sexual approach conditioning: tests of unconditioned stimulus devaluation using hormone manipulations. J. Exp. Psychol. Anim. Behav. Process. 19, 47-55.
26. Huys, Q. J., Tobler, P. N., Hasler, G., and Flagel, S. B. (2014). The role of learning-related dopamine signals in addiction vulnerability. Prog. Brain Res. 211, 31-77. doi: 10.1016/B978-0-444-63425-2.00003-9.
27. Kearns, D. N., Gomez-Serrano, M. A., Weiss, S. J., and Riley, A. L. (2006). A comparison of Lewis and Fischer rat strains on autoshaping (sign-tracking), discrimination reversal learning and negative auto-maintenance. Behav. Brain Res. 169, 193-200. doi: 10.1016/j.bbr.2006.01.005.
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. McGinty, V. B., Lardeux, S., Taha, S. A., Kim, J. J., and Nicola, S. M. (2013). Invigoration of reward seeking by cue and proximity encoding in the nucleus accumbens. Neuron 78, 910-922. doi: 10.1016/j.neuron.2013.04.010.
30. Meffre, J., Fields, H., and Ambroggi, F. (2015). "Behavioral responding in the discriminative stimulus task is habitual," in Society for Neuroscience Abstracts (Chicago, IL: Society for Neuroscience).
31. 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.
32. 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. Psychopharmacol. (Berl.) 219, 999-1009. doi: 10.1007/s00213-011-2429-7.
33. Morrison, S. E., and Nicola, S. M. (2014). Neurons in the nucleus accumbens promote selection bias for nearer objects. J. Neurosci. 34, 14147-14162. doi: 10.1523/JNEUROSCI.2197-14.2014.
34. Morrison, S. E., and Salzman, C. D. (2009). The convergence of information about rewarding and aversive stimuli in single neurons. J. Neurosci. 29, 11471-11483. doi: 10.1523/JNEUROSCI.1815-09.2009.
35. Nicola, S. M., Yun, I. A., Wakabayashi, K. T., and Fields, H. L. (2004). Cue-evoked firing of nucleus accumbens neurons encodes motivational significance during a discriminative stimulus task. J. Neurophysiol. 91, 1840-1865. doi: 10.1152/jn.00657.2003.
36. Parkinson, J. A., Dalley, J. W., Cardinal, R. N., Bamford, A., Fehnert, B., Lachenal, G., et al. (2002). Nucleus accumbens dopamine depletion impairs both acquisition and performance of appetitive Pavlovian approach behaviour: implications for mesoaccumbens dopamine function. Behav. Brain Res. 137, 149-163. doi: 10.1016/S0166-4328(02)00291-7.
37. Pickens, C. L., Saddoris, M. P., Setlow, B., Gallagher, M., Holland, P. C., and Schoenbaum, G. (2003). Different roles for orbitofrontal cortex and basolateral amygdala in a reinforcer devaluation task. J. Neurosci. 23, 11078-11084.
38. 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.
39. Robinson, T. E., Yager, L. M., Cogan, E. S., and Saunders, B. T. (2014). On the motivational properties of reward cues: individual differences. Neuropharmacology 76(Pt B), 450-459. doi: 10.1016/j.neuropharm.2013.05.040.
40. Saunders, B. T., and Robinson, T. E. (2011). Individual variation in the motivational properties of cocaine. Neuropsychopharmacology 36, 1668-1676. doi: 10.1038/npp.2011.48.
41. 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.
42. Saunders, B. T., and Robinson, T. E. (2013). Individual variation in resisting temptation: implications for addiction. Neurosci. Biobehav. Rev. 37, 1955-1975. doi: 10.1016/j.neubiorev.2013.02.008.
43. 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.
44. Tomie, A., Grimes, K. L., and Pohorecky, L. A. (2008). Behavioral characteristics and neurobiological substrates shared by Pavlovian sign-tracking and drug abuse. Brain Res. Rev. 58, 121-135. doi: 10.1016/j.brainresrev.2007.12.003.
45. Tunstall, B. J., and Kearns, D. N. (2015). Sign-tracking predicts increased choice of cocaine over food in rats. Behav. Brain Res. 281, 222-228. doi: 10.1016/j.bbr.2014.12.034.
46. Yun, I. A., Wakabayashi, K. T., Fields, H. L., and Nicola, S. M. (2004). The ventral tegmental area is required for the behavioral and nucleus accumbens neuronal firing responses to incentive cues. J. Neurosci. 24, 2923-2933. doi: 10.1523/JNEUROSCI.5282-03.2004.