Environmental rearing effects on impulsivity and reward sensitivity

Behavioral Neuroscience

Volumn 127, Issue 5, 2013, Pages 712-724

  Kirkpatrick, Kimberly ^a   Marshall, Andrew T ^a   Clarke, Jacob ^a   Cain, Mary E ^a  

^a KANSAS STATE UNIVERSITY   (United States)

Author keywords

Environmental enrichment; Impulsive action; Impulsive choice; Isolation rearing; Reward processing

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DECISION MAKING; DISCRIMINATION LEARNING; ENVIRONMENTAL FACTOR; IMPULSIVENESS; LOCOMOTION; MALE; MENTAL TASK; MOTIVATION; NONHUMAN; RAT; REARING; REINFORCEMENT; REWARD SENSITIVITY; SOCIAL ADAPTATION; SOCIAL ATTITUDE; TASK PERFORMANCE;

ANIMALS; CHOICE BEHAVIOR; ENVIRONMENT; IMPULSIVE BEHAVIOR; MALE; RATS; RATS, SPRAGUE-DAWLEY; REWARD;

EID: 84887519040     PISSN: 07357044     EISSN: 19390084     Source Type: Journal    
DOI: 10.1037/a0034124     Document Type: Article

References (64)

1. Barbelivien, A., Billy, E., Lazarus, C., Kelche, C., & Majchrzak, M. (2008). Rats with different profiles of impulsive choice behavior exhibit differences in responses to caffeine and d-amphetamine and in medial prefrontal cortex 5-HT utilization. Behavioural Brain Research, 187, 273-283. doi:10.1016/j.bbr.2007.09.020
2. Bardo, M. T., Bowling, S. L., Rowlett, J. K., Manderscheid, P., Buxton, S. T., & Dwoskin, L. P. (1995). Environmental enrichment attenuates locomotor sensitization, but not in vitro dopamine release, induced by amphetamine. Pharmacology Biochemistry and Behavior, 51, 397-405. doi:10.1016/0091-3057(94)00413-D
3. Bardo, M. T., & Dwoskin, L. P. (2004). Biological connection between novelty-and drug-seeking motivational systems. Nebraska Symposium on Motivation, 50, 127-158.
4. Bardo, M. T., Valone, J., Robinet, P. M., Buxton, S. T., Shaw, W., & Dwoskin, L. P. (1999). Environmental enrichment enhances the stimulant effect of intravenous amphetamine: Search for a cellular mechanism in the nucleus accumbens. Psychobiology, 27, 292-299.
5. Bari, A., Theobald, D. E., Caprioli, D., Mar, A. C., Aidoo-Micah, A., Dalley, J. W., & Robbins, T. W. (2010). Serotonin modulates sensitivity to reward and negative feedback in a probabilistic reversal learning task in rats. Neuropsychopharmacology, 35, 1290-1301. doi:10.1038/npp .2009.233
6. Bateson, M., & Kacelnik, A. (1995). Preferences for fixed and variable food sources: Variability in amount and delay. Journal of the Experimental Analysis of Behavior, 63, 313-329. doi:10.1901/jeab.1995.63-313
7. Beckmann, J. S., & Bardo, M. T. (2012). Environmental enrichment reduces attribution of incentive salience to a food-associated stimulus. Behavioural Brain Research, 226, 331-334. doi:10.1016/j.bbr.2011.09.021
8. Bowling, S. L., Rowlett, J. K., & Bardo, M. T. (1993). The effect of environmental enrichment on amphetamine-stimulated locomotor activ- ity, dopamine synthesis and dopamine release. Neuropharmacology, 32, 885-893. doi:10.1016/0028-3908(93)90144-R
9. Brenes, J. C., & Fornaguera, J. (2008). Effects of environmental enrichment and social isolation on sucrose consumption and preference: Associations with depressive-like behavior and ventral striatum dopamine. Neuroscience Letters, 436, 278-282. doi:10.1016/j.neulet.2008.03.045
10. Brenes, J. C., Padilla, M., & Fornaguera, J. (2009). A detailed analysis of open-field habituation and behavioral and neurochemical antidepressantlike effects in postweaning enriched rats. Behavioural Brain Research, 197, 125-137.
11. Brenes, J. C., Rodríguez, O., & Fornaguera, J. (2008). Differential effect of environment enrichment and social isolation on depressive-like behavior, spontaneous activity and serotonin and norepinephrine concentration in prefrontal cortex and ventral striatum. Pharmacology Biochemistry and Behavior, 89, 85-93. doi:10.1016/j.pbb.2007.11.004
12. Brunner, D., & Hen, R. (1997). Insights into the neurobiology of impulsive behavior from serotonin receptor knockout mice. Annals of the New York Academy of Sciences, 836, 81-105. doi:10.1111/j.1749-6632.1997.tb52356.x
13. Cain, M. E., Green, T. A., & Bardo, M. T. (2006). Environmental enrichment decreases responding for visual novelty. Behavioural Processes, 73, 360-366. doi:10.1016/j.beproc.2006.08.007
14. Cain, M. E., Mersmann, M. G., Gill, M. J., & Pittenger, S. T. (2012). Dose-dependent effects of differential rearing on amphetamine-induced hyperactivity. Behavioural Pharmacology, 23, 744-753. doi:10.1097/FBP.0b013e32835a38ec
15. Cardinal, R. N., Pennicott, D. R., Sugathapala, C. L., Robbins, T. W., & Everitt, B. J. (2001, June 29). Impulsive choice induced in rats by lesions of the nucleus accumbens core. Science, 292, 2499-2501. doi:10.1126/science.1060818
16. Catania, A. C. (1970). Reinforcement schedules and psychophysical judgments. In W. N. Schoenfeld (Ed.), Theory of reinforcement schedules (pp. 1-42). New York, NY: Appleton-Century-Crofts.
17. Coolon, R. A., & Cain, M. E. (2009). Effects of mecamylamine on nicotine-induced conditioned hyperactivity and sensitization in differentially reared rats. Pharmacology Biochemistry and Behavior, 93, 59-66. doi:10.1016/j.pbb.2009.04.007
18. Dalley, J. W., Theobald, D. E., Pereira, E. A. C., Li, P. M. M. C., & Robbins, T. W. (2002). Specific abnormalities in serotonin release in the prefrontal cortex of isolation-reared rats measured during behavioural performance of a task assessing visuospatial attention and impulsivity. Psychopharmacology, 164, 329-340. doi:10.1007/s00213-002-1215-y
19. Deehan, G. A., Cain, M. E., & Kiefer, S. W. (2007). Differential rearing conditions alter operant responding for ethanol in outbred rats. Alcoholism:Clinical and Experimental Research, 31, 1692-1698. doi:10.1111/j.1530-0277.2007.00466.x
20. Deehan, G. A., Palmatier, M. I., Cain, M. E., & Kiefer, S. W. (2011). Differential rearing conditions and alcohol-preferring rats: Consumption of and operant responding for ethanol. Behavioral Neuroscience, 125, 184-193. doi:10.1037/a0022627
21. Diergaarde, L., Pattij, T., Poortvliet, I., Hogenboom, F., de Vries, W., Schoffelmeer, A. N. M., & De Vries, T. J. (2008). Impulsive choice and impulsive action predict vulnerability to distinct stages of nicotine seeking in rats. Biological Psychiatry, 63, 301-308. doi:10.1016/j .biopsych.2007.07.011
22. Evenden, J. L. (1999). Varieties of impulsivity. Psychopharmacology, 146, 348-361. doi:10.1007/PL00005481
23. Fone, K. C. F., & Porkess, M. V. (2008). Behavioural and neurochemical effects of post-weaning social isolation in rodents-Relevance to development neuropsychiatric disorders. Neuroscience and Biobehavioral Reviews, 32, 1087-1102. doi:10.1016/j.neubiorev.2008.03.003
24. Galtress, T., Garcia, A., & Kirkpatrick, K. (2012). Individual differences in impulsive choice and timing in rats. Journal of the Experimental Analysis of Behavior, 98, 65-87. doi:10.1901/jeab.2012.98-65
25. Galtress, T., & Kirkpatrick, K. (2010). The role of the nucleus accumbens core in impulsive choice, timing, and reward processing. Behavioral Neuroscience, 124, 26-43. doi:10.1037/a0018464
26. Garcia, A., & Kirkpatrick, K. (2013). Impulsive choice behavior in four strains of rats: Evaluation of possible models of attention-deficit/hyperactivity disorder. Behavioural Brain Research, 238, 10-22. doi:10.1016/j.bbr.2012.10.017
27. Gill, M. J., Arnold, J. C., & Cain, M. E. (2012). Impact of mGluR5 during amphetamine-induced hyperactivity and conditioned hyperactivity in differentially reared rats. Psychopharmacology, 221, 227-237. doi:10.1007/s00213-011-2565-0
28. Gill, M. J., & Cain, M. E. (2011). Effects of satiety on operant responding in rats raised in enrichment. Behavioural Pharmacology, 22, 40-48. doi:10.1097/FBP.0b013e3283425a86
29. Green, L., & Estle, S. J. (2003). Preference reversals with food and water reinforcers in rats. Journal of the Experimental Analysis of Behavior, 79, 233-242. doi:10.1901/jeab.2003.79-233
30. Green, T. A., Gehrke, B. J., & Bardo, M. T. (2002). Environmental enrichment decreases intravenous amphetamine self-administration in rats: Dose-response functions for fixed- and progressive-ratio schedules. Psychopharmacology, 162, 373-378. doi:10.1007/s00213-002-1134-y
31. Hellemans, K. G. C., Nobrega, J. N., & Olmstead, M. C. (2005). Early environmental experience alters baseline and ethanol-induced cognitive impulsivity: Relationship to forebrain 5-HT1A receptor binding. Behavioural Brain Research, 159, 207-220. doi:10.1016/j.bbr.2004.10.018
32. Hill, J. C., Covarrubias, P., Terry, J., & Sanabria, F. (2012). The effect of methylphenidate and rearing environment on behavioral inhibition in adult male rats. Psychopharmacology, 219, 353-362. doi:10.1007/s00213-011-2552-5
33. Ho, M.-Y., Al-Zahrani, S. S. A., Al-Ruwaitea, A. S. A., Bradshaw, C. M., & Szabadi, E. (1998). 5-hydroxytryptamine and impulse control: Prospects for a behavioural analysis. Journal of Psychopharmacology, 12, 67-78. doi:10.1177/026988119801200109
34. Ikemoto, S., & Panksepp, J. (1999). The role of nucleus accumbens dopamine in motivated behavior: A unifying interpretation with special reference to reward-seeking. Brain Research Reviews, 31, 6-41. doi:10.1016/S0165-0173(99)00023-5
35. Jones, G. H., Marsden, C. A., & Robbins, T. W. (1990). Increased sensitivity to amphetamine and reward-related stimuli following social isolation in rats: Possible disruption of dopamine-dependent mechanisms of the nucleus accumbens. Psychopharmacology, 102, 364-372. doi:10.1007/BF02244105
36. Kacelnik, A., Vasconcelos, M., Monteiro, T., & Aw, J. (2011). Darwin's "tug-of-war" vs. starlings' "horse-racing": How adaptations for sequential encounters drive simultaneous choice. Behavioral Ecology and Sociobiology, 65, 547-558. doi:10.1007/s00265-010-1101-2
37. Lapiz, M. D. S., Fulford, A., Muchimapura, S., Mason, R., Parker, T., & Marsden, C. A. (2003). Influence of postweaning social isolation in the rat on brain development, conditioned behavior, and neurotransmission. Neuroscience and Behavioral Physiology, 33, 13-29. doi:10.1023/A:1021171129766
38. Loos, M., Pattij, T., Janssen, M. C., Counotte, D. S., Schoffelmeer, A. N., Smit, A. B.,.. van Gaalen, M. M. (2010). Dopamine receptor D1/D5 gene expression in the medial prefrontal cortex predicts impulsive choice in rats. Cerebral Cortex, 20, 1064-1070. doi:10.1093/cercor/bhp167
39. Lore, R. K., & Levowitz, A. (1966). Differential rearing and free versus forced exploration. Psychonomic Science, 5, 421-422.
40. Morgan, M., & Einon, D. (1975). Incentive motivation and behavioral inhibition in socially-isolated rats. Physiology & Behavior, 15, 405-409. doi:10.1016/0031-9384(75)90250-4
41. Odum, A. L. (2011). Delay discounting: I'm a k, you're a k. Journal of the Experimental Analysis of Behavior, 96, 427-439. doi:10.1901/jeab.2011.96-423
42. Ough, B. R., Beatty, W. W., & Khalili, J. (1972). Effects of isolated and enriched rearing on response inhibition. Psychonomic Science, 27, 293-294.
43. Pardey, M. C., Kumar, N. N., Goodchild, A. K., & Cornish, J. L. (2012). Catecholamine receptors differentially mediate impulsive choice in the medial prefrontal and orbitofrontal cortex. Journal of Psychopharmacology, 27, 203-212. doi:0269881112465497
44. Perry, J. L., Stairs, D. J., & Bardo, M. T. (2008). Impulsive choice and environmental enrichment: Effects of d-amphetamine and methylphenidate. Behavioural Brain Research, 193, 48-54. doi:10.1016/j.bbr.2008.04.019
45. Rahman, S., & Bardo, M. T. (2008). Environmental enrichment increases amphetamine-induced glutamate neurotransmission in the nucleus accumbens:A neurochemical study. Brain Research, 1197, 40-46. doi:10.1016/j.brainres.2007.12.052
46. Reboreda, J. C., & Kacelnik, A. (1991). Risk sensitivity in starlings:Variability in food amount and delay. Behavioral Ecology, 2, 301-308. doi:10.1093/beheco/2.4.301
47. Renner, M. J., & Rosenzweig, M. R. (1987). Enriched and impoverished environments: Effects on brain and behavior. New York, NY: Springer-Verlag. doi:10.1007/978-1-4612-4766-1
48. Roberts, S. (1981). Isolation of an internal clock. Journal of Experimental Psychology: Animal Behavior Processes, 7, 242-268. doi:10.1037/0097-7403.7.3.242
49. Roesch, M. R., Calu, D. J., & Schoenbaum, G. (2007). Dopamine neurons encode the better option in rats deciding between differently delayed or sized rewards. Nature Neuroscience, 10, 1615-1624. doi:10.1038/nn2013
50. Shapiro, M. S., Siller, S., & Kacelnik, A. (2008). Simultaneous and sequential choice as a function of reward delay and magnitude: Normative, descriptive and process-based models tested in the European starling (Sturnus vulgaris). Journal of Experimental Psychology: Animal Behavior Processes, 34, 75-93. doi:10.1037/0097-7403.34.1.75
51. Simpson, J., & Kelly, J. P. (2011). The impact of environmental enrichment in laboratory rats-Behavioural and neurochemical aspects. Behavioural Brain Research, 222, 246-264. doi:10.1016/j.bbr.2011.04.002
52. Smith, J. K., Neill, J. C., & Costall, B. (1997). Post-weaning housing conditions influence the behavioural effects of cocaine and d-amphetamine. Psychopharmacology, 131, 23-33. doi:10.1007/s002130050261
53. Smith, M. A., Bryant, P. A., & McClean, J. M. (2003). Social and environmental enrichment enhances sensitivity to the effects of kappa opioids: Studies on antinociception, diuresis and conditioned place preference. Pharmacology Biochemistry and Behavior, 76, 93-101. doi:10.1016/S0091-3057(03)00189-8
54. Smith, M. A., Chisholm, K. A., Bryant, P. A., Greene, J. L., McClean, J. M., Stoops, W. W., & Yancey, D. L. (2005). Social and environmental influences on opioid sensitivity in rats: Importance of an opioid's relative efficacy at the mu-receptor. Psychopharmacology, 181, 27-37. doi:10.1007/s00213-005-2218-2
55. Stairs, D. J., & Bardo, M. T. (2009). Neurobehavioral effects of environmental enrichment and drug abuse vulnerability. Pharmacology Biochemistry and Behavior, 92, 377-382. doi:10.1016/j.pbb.2009.01.016
56. Tatham, T. A., & Zurn, K. R. (1989). The MED-PC experimental apparatus programming system. Behavior Research Methods, Instruments, & Computers, 21, 294-302. doi:10.3758/BF03205598
57. van der Harst, J. E., Baars, A.-M., & Spruijt, B. M. (2003). Standard housed rats are more sensitive to rewards than enriched house rats as reflected by their anticipatory behaviour. Behavioural Brain Research, 142, 151-156. doi:10.1016/S0166-4328(02)00403-5
58. Wood, D. A., Buse, J. E., Wellman, C. L., & Rebec, G. V. (2005). Differential environmental exposure alters NMDA but not AMPA receptor subunit expression in nucleus accumbens core and shell. Brain Research, 1042, 176-183. doi:10.1016/j.brainres.2005.02.029
59. Wood, D. A., & Rebec, G. V. (2009). Environmental enrichment alters neuronal processing in the nucleus accumbens core during appetitive conditioning. Brain Research, 1259, 59-67. doi:10.1016/j.brainres.2008.12.038
60. Wood, D. A., Siegel, A. K., & Rebec, G. V. (2006). Environmental enrichment reduces impulsivity during appetitive conditioning. Physiology & Behavior, 88, 132-137. doi:10.1016/j.physbeh.2006.03.024
61. Wooters, T. E., Bardo, M. T., Dwoskin, L. P., Midde, N. M., Gomez, A. M., Mactutus, C. F.,.. Zhu, J. (2011). Effect of environmental enrichment on methylphenidate-induced locomotion and dopamine transporter dynamics. Behavioural Brain Research, 219, 98-107. doi:10.1016/j.bbr.2011.01.001
62. Zeeb, F. D., Wong, A. C., & Winstanley, C. A. (2013). Differential effects of environmental enrichment, social-housing, and isolation-rearing on a rat gambling task: Dissociations between impulsive action and risky decision-making. Psychopharmacology, 225, 381-395. doi:10.1007/s00213-012-2822-x
63. Zhu, J., Apparsundaram, S., Bardo, M. T., & Dwoskin, L. P. (2005). Environmental enrichment decreases cell surface expression of the dopamine transporter in rat medial prefrontal cortex. Journal of Neurochemistry, 93, 1434-1443. doi:10.1111/j.1471-4159.2005.03130.x
64. Zimmermann, A., Stauffacher, M., Langhans, W., & Würbel, H. (2001). Enrichment-dependent differences in novelty exploration in rats can be explained by habituation. Behavioural Brain Research, 121, 11-20. doi:10.1016/S0166-4328(00)00377-6