A rodent version of the Iowa Gambling Task: 7 years of progress

Frontiers in Psychology

Volumn 5, Issue MAR, 2014, Pages

  Van den Bos, Ruud ^a   Koot, Susanne ^b,c   De Visser, Leonie ^c,d  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d Excerpta Medica   (United States)

Author keywords

Behavioral models; Decision making; Foraging behavior; Humans; Prefrontal cortex; Rats

Indexed keywords

EID: 84897493990     PISSN: None     EISSN: 16641078     Source Type: Journal    
DOI: 10.3389/fpsyg.2014.00203     Document Type: Review

References (72)

1. Bechara, A. (2005). Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective. Nat. Neurosci. 8, 1458-1463. doi: 10.1038/nn1584
2. Bechara, A., Damasio, A. R., Damasio, H., and Anderson, S. W. (1994). Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50, 7-15. doi: 10.1016/0010-0277(94)90018-3
3. Bechara, A., Damasio, H., Damasio, A. R., and Lee, G. P. (1999). Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making. J. Neurosci. 19, 5473-5481.
4. Bechara, A., Damasio, H., Tranel, D., and Damasio, A. R. (1997). Deciding advantageously before knowing the advantageous strategy. Science 275, 1293-1295. doi: 10.1126/science.275.5304.1293
5. Burgos-Robles, A., Bravo-Rivera, H., and Quirk, G. J. (2013). Prelimbic and infralimbic neurons signal distinct aspects of appetitive instrumental behavior. PLoS ONE 8:e57575. doi: 10.1371/journal.pone.0057575
6. Butti, C., and Hof, P. R. (2010). The insular cortex: a comparative perspective. Brain Struct. Funct. 214, 477-493. doi: 10.1007/s00429-010-0264-y
7. Cabanac, M. (1971). Physiological role of pleasure. Science 173, 1103-1107. doi: 10.1126/science.173.4002.1103
8. Cabanac, M. (1992). Pleasure: the common currency. J. Theor. Biol. 155, 173-200. doi: 10.1016/S0022-5193(05)80594-6
9. Clark, L., Bechara, A., Damasio, H., Aitken, M. R., Sahakian, B. J., and Robbins, T. W. (2008). Differential effects of insular and ventromedial prefrontal cortex lesions on risky decision-making. Brain 131, 1311-1322. doi: 10.1093/brain/awn066
10. Cowen, S. L., Davis, G. A., and Nitz, D. A. (2012). Anterior cingulate neurons in the rat map anticipated effort and reward to their associated action sequences. J. Neurophysiol. 107, 2393-2407. doi: 10.1152/jn.01012.2011
11. Craig, A. D. (2011). Significance of the insula for the evolution of human awareness of feelings from the body. Ann. N. Y. Acad. Sci. 1225, 72-82. doi: 10.1111/j.1749-6632.2011.05990.x
12. Croxson, P. L., Walton, M. E., O'Reilly, J. X., Behrens, T. E. J., and Rushworth, M. F. S. (2009). Effort-Based cost-benefit valuation and the human brain. J. Neurosci. 29, 4531-4541. doi: 10.1523/JNEUROSCI.4515-08.2009
13. Damasio, A. R. (1994). Descartes' Error. Emotion, Reason and the Human Brain. New York: Avon Books.
14. de Visser, L. (2003). Risk-Sensitive Foraging: The Theory so far. MSc thesis, Utrecht University, Utrecht, The Netherlands.
15. de Visser, L., Homberg, J. R., Mitsogiannis, M., Zeeb, F. D., Rivalan, M., Fitoussi, A., et al. (2011a). Rodent versions of the iowa gambling task: opportunities and challenges for the understanding of decision-making. Front. Neurosci. 5:109. doi: 10.3389/fnins.2011.00109
16. de Visser, L., Baars, A. M., Lavrijsen, M., van der Weerd, C. M., and van den Bos, R. (2011b). Decision-making performance is related to levels of anxiety and differential recruitment of frontostriatal areas in male rats. Neuroscience 184, 97-106. doi: 10.1016/j.neuroscience.2011.02.025
17. de Visser, L., Baars, A. M., van 't Klooster, J., and van den Bos, R. (2011c). Transient inactivation of the medial prefrontal cortex affects both anxiety and decision-making in male wistar rats. Front. Neurosci. 5:102. doi: 10.3389/fnins.2011.00102
18. de Visser, L., van der Knaap, L. J., van de Loo, A. J., van der Weerd, C. M., Ohl, F., and van den Bos, R. (2010). Trait anxiety affects decision-making differently in healthy men and women: towards gender-specific endophenotypes of anxiety. Neuropsychologia 48, 1598-1606. doi: 10.1016/j.neuropsychologia.2010.01.027
19. Dunn, B. D., Dalgleish, T., and Lawrence, A. D. (2006). The somatic marker hypothesis: a critical evaluation. Neurosci. Biobehav. Rev. 30, 239-271. doi: 10.1016/j.neubiorev.2005.07.001
20. Gass, J. T., and Chandler, L. J. (2013). The plasticity of extinction: contribution of the prefrontal cortex in treating addiction through inhibitory learning. Front. Psychiatry 4:46. doi: 10.3389/fpsyt.2013.00046
21. Gläscher, J., Adolphs, R., Damasio, H., Bechara, A., Rudrauf, D., Calamia, M., et al. (2012). Lesion mapping of cognitive control and value-based decision making in the prefrontal cortex. Proc. Natl. Acad. Sci. U.S.A. 109, 14681-14686. doi: 10.1073/pnas.1206608109
22. Homberg, J. R., van den Bos, R., den Heijer, E., Suer, R., and Cuppen, E. (2008). Serotonin transporter dosage modulates long-term decision-making in rat and human. Neuropharmacology 55, 80-84. doi: 10.1016/j.neuropharm.2008.04.016
23. Horst, N. K., and Laubach, M. (2013). Reward-related activity in the medial prefrontal cortex is driven by consumption. Front. Neurosci. 7:56. doi: 10.3389/fnins.2013.00056
24. Inglis, I. R., Forkman, B., and Lazarus, J. (1997). Free food or earned food? A review and fuzzy model of contrafreeloading. Anim. Behav. 53, 1171-1191. doi: 10.1006/anbe.1996.0320
25. Inglis, I. R., Langton, S., Forkman, B., and Lazarus, J. (2001). An information primacy model of exploratory and foraging behaviour. Anim. Behav. 62, 543-557. doi: 10.1006/anbe.2001.1780
26. Ishii, H., Ohara, S., Tobler, P. N., Tsutsui, K.-I., and Iijima, T. (2012). Inactivating anterior insular cortex reduces risk taking. J. Neurosci. 32, 16031-16039. doi: 10.1523/JNEUROSCI.2278-12.2012
27. Killcross, S., and Coutureau, E. (2003). Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb. Cortex 13, 400-408. doi: 10.1093/cercor/13.4.400
28. Kolling, N., Behrens, T. E. J., Mars, R. B., and Rushworth, M. F. S. (2012). Neural mechanisms of foraging. Science 336, 95-98. doi: 10.1126/science.1216930
29. Koot, S., Adriani, W., Saso, L., van den Bos, R., and Laviola, G. (2009a). Home cage testing of delay discounting in rats. Behav. Res. Methods 41, 1169-1176. doi: 10.3758/BRM.41.4.1169
30. Koot, S., van den Bos, R., Adriani, W., and Laviola, G. (2009b). Gender differences in delay-discounting under mild food restriction. Behav. Brain Res. 200, 134-143. doi: 10.1016/j.bbr.2009.01.006
31. Koot, S., Baars, A., Hesseling, P., van den Bos, R., and Joëls, M. (2013). Time-dependent effects of corticosterone on reward-based decision-making in a rodent model of the Iowa gambling task. Neuropharmacology 70, 306-315. doi: 10.1016/j.neuropharm.2013.02.008
32. Koot, S., Koukou, M., Baars, A., Hesseling, P., van 't Klooster, J., Joëls, M., et al. (2014). Corticosterone and decision-making in male Wistar rats: the effect of corticosterone application in the infralimbic and orbitofrontal cortex. Available at: http://www.frontiersin.org/Journal/abstract/73779
33. Koot, S., Zoratto, F., Cassano, T., Colangeli, R., Laviola, G., van den Bos, R., et al. (2012). Compromised decision-making and increased gambling proneness following dietary serotonin depletion in rats. Neuropharmacology 62, 1640-1650. doi: 10.1016/j.neuropharm.2011.11.002
34. Kravitz, A. K., Tye, L. D., and Kreitzer, A. C. (2012). Distinct roles for direct and indirect pathway striatal neurons in reinforcement. Nat. Neurosci. 15, 816-818. doi: 10.1038/nn.3100
35. Krebs, J. R., and Davies, N. B. (1993). An Introduction to Behavioural Ecology, 3rd Edn. Oxford: Blackwell Scientific Publications.
36. Lawrence, N. S., Jollant, F., O'Daly, O., Zelaya, F., and Phillips, M. L. (2009). Distinct roles of prefrontal cortical subregions in the iowa gambling task. Cereb. Cortex 154, 1134-1143. doi: 10.1093/cercor/bhn154
37. Li, X., Lu, Z.-L., D'Argembeau, A., Ng, M., and Bechara, A. (2010). The Iowa gambling task in fMRI Images. Hum. Brain Mapp. 31, 410-423.
38. Lin, C.-H., Chiu, Y.-C., Cheng, C.-M., and Hsieh, J. C. (2008). Brain maps of Iowa gambling task. BMC Neurosci. 9:72. doi: 10.1186/1471-2202-9-72
39. McClure, S. M., Laibson, D. I., Loewenstein, G., and Cohen, J. D. (2004). Separate neural systems value immediate and delayed monetary rewards. Science 306, 503-507. doi: 10.1126/science.1100907
40. Mihindou, C., Guillem, K., Navailles, S., Vouiilac, C., and Ahmed, S. (2013). Discriminative inhibitory control of cocaine seeking involves the prelimbic prefrontal cortex. Biol. Psychiatry 73, 271-279. doi: 10.1016/j.biopsych.2012.08.011
41. Milad, M. R., and Quirk, G. J. (2012). Fear Extinction as a model for translational neuroscience: ten years of progress. Annu. Rev. Psychol. 63, 129-151. doi: 10.1146/annurev.psych.121208.131631
42. Northoff, G., Grimm, S., Boeker, H., Schmidt, C., Bermpohl, F., Heinzel, A., et al. (2006). Affective judgment and beneficial decision making: ventromedial prefrontal activity correlates with performance in the iowa gambling task. Hum. Brain Mapp. 27, 572-587. doi: 10.1002/hbm.20202
43. Ostlund, S. B., and Balleine, B. W. (2005). Lesions of medial prefrontal cortex disrupt the acquisition but not the expression of goal-directed learning. J. Neurosci. 25, 7763-7770. doi: 10.1523/JNEUROSCI.1921-05.2005
44. Paine, T. A., Asinof, S. K., Diehl, G. W., Frackman, A., and Leffler, J. (2013). Medial prefrontal cortex lesions impair decision-making on a rodent gambling task: reversal by D1 receptor antagonist administration Behav. Brain Res. 243, 247-254. doi: 10.1016/j.bbr.2013.01.018
45. Pais-Vieira, M., Lima, D., and Galhardo, V. (2007). Orbitofrontal cortex lesions disrupt risk assessment in a novel serial decision-making task for rats. Neuroscience 145, 225-231. doi: 10.1016/j.neuroscience.2006.11.058
46. Paton, J. J., and Louie, K. (2012). Reward and punishment illuminated. Nat. Neurosci. 5, 807-809. doi: 10.1038/nn.3122
47. Pittaras, E., Cressant, A., Serreau, P., Bruijel, J., Dellu-Hagedorn, F., Callebert, J., et al. (2013). Mice gamble for food: Individual differences in risky choices and prefrontal cortex serotonin. J. Addict. Res. Ther. S4:011. doi: 10.4172/2155-6105.S4-011
48. Prévost, C., Pessiglione, M., Météreau, E., Cléry-Melin, M. L., and Dreher, J. C. (2010). Separate valuation subsystems for delay and effort decision costs. J. Neurosci. 30, 14080-14090. doi: 10.1523/JNEUROSCI.2752-10.2010
49. Proctor, D. (2012). Gambling and Decision-Making Among Primates: The Primate Gambling Task. Ph.D. thesis, Psychology Dissertations, Paper 108, Georgia State University, Atlanta, GA. Available at: http://digitalarchive.gsu.edu/psych_diss/108
50. Rivalan, M., Ahmed, S. H., and Dellu-Hagedorn, F. (2009). Risk-prone individuals prefer the wrong options on a rat version of the Iowa gambling task. Biol. Psychiatry 66, 743-749. doi: 10.1016/j.biopsych.2009.04.008
51. Rivalan, M., Coutureau, E., Fitoussi, A., and Dellu-Hagedorn, F. (2011). Inter-individual decision-making differences in the effects of cingulate, orbitofrontal, and prelimbic cortex lesions in a rat gambling task. Front. Behav. Neurosci. 5:22. doi: 10.3389/fnbeh.2011.00022
52. Roy, M., Shohamy, D., and Wager, T. D. (2012). Ventromedial prefrontal-subcortical systems and the generation of affective meaning. Trends Cogn. Sci. 16, 147-156. doi: 10.1016/j.tics.2012.01.005
53. Rudebeck, P. H., Walton, M. E., Smyth, A. N., Bannerman, D. M., and Rushworth, M. F. (2006). Separate neural pathways process different decision costs. Nat. Neurosci. 9, 1161-1168. doi: 10.1038/nn1756
54. Spruijt, B. M., van den Bos, R., and Pijlman, F. T. A. (2001). A concept of welfare based on reward evaluating mechanisms in the brain: anticipatory behaviour as an indicator for the state of reward systems. Appl. Anim. Behav. Sci. 72, 145-171. doi: 10.1016/S0168-1591(00)00204-5
55. Tanaka, S. C., Doya, K., Okada, G., Ueda, K., Okamoto, Y., and Yamawaki, S. (2004). Prediction of immediate and future rewards differentially recruits cortico-basal ganglia systems. Nat. Neurosci. 7, 887-893. doi: 10.1038/nn1279
56. van den Bos, R. (2004). "Emotion and cognition," in The Handbook of Animal Behavior, ed. M. Bekoff (Westport, CT: Greenwood Press), 554-557.
57. van den Bos, R., and de Ridder, D. (2006). Evolved to satisfy our immediate needs: Self-control and the rewarding properties of food. Appetite 47, 24-29. doi: 10.1016/j.appet.2006.02.008
58. van den Bos, R., Lasthuis, W., den Heijer, E., van der Harst, J., and Spruijt, B. (2006a). Toward a rodent model of the Iowa gambling task. Behav. Res. Methods 38, 470-478. doi: 10.3758/BF03192801
59. van den Bos, R., Houx, B. B., and Spruijt, B. M. (2006b). The effect of reward magnitude differences on choosing disadvantageous decks in the Iowa gambling task. Biol. Psychol. 71, 155-161. doi: 10.1016/j.biopsycho.2005.05.003
60. van den Bos, R., van der Harst, J., Jonkman, S., Schilders, M., and Spruijt, B. (2006c). Rats assess costs and benefits according to an internal standard. Behav. Brain Res. 171, 350-354. doi: 10.1016/j.bbr.2006.03.035
61. van den Bos, R., Jolles, J., van der Knaap, L., Baars, A., and de Visser, L. (2012). Male and female Wistar rats differ in decision-making performance in a rodent version of the Iowa Gambling Task. Behav. Brain Res. 234, 375-379. doi: 10.1016/j.bbr.2012.07.015
62. van den Bos, R., Davies, W., Dellu-Hagedorn, F., Goudriaan, A. E., Granon, S., Homberg, J., et al. (2013a). Cross-species approaches to pathological gambling: a review targeting sex differences, adolescent vulnerability and ecological validity of research tools. Neurosci. Biobehav. Rev. 37, 2454-2471. doi: 10.1016/j.neubiorev.2013.07.005
63. van den Bos, R., Homberg, J., and de Visser, L. (2013b). A critical review of sex differences in decision-making tasks: focus on the Iowa gambling task. Behav. Brain Res. 238, 95-108. doi: 10.1016/j.bbr.2012.10.002
64. van den Bos, R., Jolles, J. W., and Homberg, J. (2013c). Social modulation of decision-making: a cross species review. Front. Hum. Neurosci. 7:301. doi: 10.3389/fnhum.2013.00301
65. van Hasselt, F. N., de Visser, L., Tieskens, J. M., Cornelisse, S., Baars, A. M., Lavrijsen, M., et al. (2012). Individual variations in maternal care early in life correlate with later life decision-making and c-fos expression in prefrontal subregions of rats. PLoS ONE 7:e37820. doi: 10.1371/journal.pone.0037820
66. Walton, M. E., Bannerman, D. M., Alterescu, K., and Rushworth, M. F. (2003). Functional specialization within medial frontal cortex of the anterior cingulate for evaluating effort-related decisions. J. Neurosci. 23, 6475-6479.
67. Xue, G., Lu, Z., Levin, I. P., and Bechara, A. (2010). The impact of prior risk experiences on subsequent risky decision-making: the role of the insula. Neuroimage 50, 709-716. doi: 10.1016/j.neuroimage.2009.12.097
68. Yin, H. H., and Knowlton, B. J. (2006). The role of the basal ganglia in habit formation. Nat. Rev. Neurosci. 7, 464-476. doi: 10.1038/nrn1919
69. Yin, H. H., Ostlund, S. B., and Balleine, B. W. (2008). Reward-guided learning beyond dopamine in the nucleus accumbens: the integrative functions of cortico-basal ganglia networks. Eur. J. Neurosci. 28, 1437-1448. doi: 10.1111/j.1460-9568.2008.06422.x
70. Zeeb, F. D., Robbins, T. W., and Winstanley, C. A. (2009). Serotonergic and dopaminergic modulation of gambling behavior as assessed using a novel rat gambling task. Neuropsychopharmacology 34, 2329-2343. doi: 10.1038/npp.2009.62
71. Zeeb, F. D., and Winstanley, C. A. (2011). Lesions of the basolateral amygdala and orbitofrontal cortex differentially affect acquisition and performance of a rodent gambling task. J. Neurosci. 31, 2197-2204. doi: 10.1523/JNEUROSCI.5597-10.2011
72. Zeeb, F. D., and Winstanley, C. A. (2013). Functional disconnection of the orbitofrontal cortex and basolateral amygdala impairs acquisition of a rat gambling task and disrupts animals' ability to alter decision-making behavior after reinforcer devaluation. J. Neurosci. 33, 6434-6443. doi: 10.1523/JNEUROSCI.3971-12.2013