A closer look at the effects of repeated cocaine exposure on adaptive decision-making under conditions that promote goal-directed control

Frontiers in Psychiatry

Volumn 7, Issue MAR, 2016, Pages

  Halbout, Briac ^a,b   Liu, Angela T ^a,b   Ostlund, Sean B ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Choice; Cognitive control; Contingency degradation; Goal directed; Habit learning; Outcome devaluation; Rat; Sensitization

Indexed keywords

COCAINE;

ADAPTIVE BEHAVIOR; ADULT; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR CONTROL; COGNITIVE BIAS; CONTINGENCY DEGRADATION; CONTROLLED STUDY; DECISION MAKING; DEVALUATION; DRUG REEXPOSURE; GOAL DIRECTED CONTROL; HABIT; HABITUAL ADAPTATION; INSTRUMENTAL CONDITIONING; LOCOMOTION; MALE; NONHUMAN; RAT; REINFORCEMENT; TASK PERFORMANCE;

EID: 84964632510     PISSN: None     EISSN: 16640640     Source Type: Journal    
DOI: 10.3389/fpsyt.2016.00044     Document Type: Article

References (75)

1. Deroche-Gamonet V, Belin D, Piazza PV. Evidence for addiction-like behavior in the rat. Science (2004) 305:1014-7. doi:10.1126/science.1099020
2. Vanderschuren LJ, Everitt BJ. Drug seeking becomes compulsive after prolonged cocaine self-administration. Science (2004) 305:1017-9. doi:10.1126/science.1098975
3. Everitt BJ, Robbins TW. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci (2005) 8:1481-9. doi:10.1038/nn1579
4. Ostlund SB, Balleine BW. On habits and addiction: an associative analysis of compulsive drug seeking. Drug Discov Today Dis Models (2008) 5:235-45. doi:10.1016/j.ddmod.2009.07.004
5. Redish AD, Jensen S, Johnson A. A unified framework for addiction: vulnerabilities in the decision process. Behav Brain Sci (2008) 31:415-37; discussion 437-87. doi:10.1017/S0140525X0800472X
6. Torregrossa MM, Corlett PR, Taylor JR. Aberrant learning and memory in addiction. Neurobiol Learn Mem (2011) 96:609-23. doi:10.1016/j.nlm.2011.02.014
7. Lucantonio F, Caprioli D, Schoenbaum G. Transition from 'model-based' to 'model-free' behavioral control in addiction: involvement of the orbitofrontal cortex and dorsolateral striatum. Neuropharmacology (2014) 76(Pt B):407-15. doi:10.1016/j.neuropharm.2013.05.033
8. Everitt BJ, Robbins TW. Drug addiction: updating actions to habits to compulsions ten years on. Annu Rev Psychol (2015) 67:23-50. doi:10.1146/annurev-psych-122414-033457
9. Balleine BW, Dickinson A. Goal-directed instrumental action: contingency and incentive learning and their cortical substrates. Neuropharmacology (1998) 37:407-19. doi:10.1016/S0028-3908(98)00033-1
10. Yin HH, Knowlton BJ. The role of the basal ganglia in habit formation. Nat Rev Neurosci (2006) 7:464-76. doi:10.1038/nrn1919
11. Balleine BW, O'Doherty JP. Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology (2010) 35:48-69. doi:10.1038/npp.2009.131
12. Liljeholm M, Tricomi E, O'Doherty JP, Balleine BW. Neural correlates of instrumental contingency learning: differential effects of action-reward conjunction and disjunction. J Neurosci (2011) 31:2474-80. doi:10.1523/JNEUROSCI.3354-10.2011
13. Liljeholm M, Dunne S, O'Doherty JP. Differentiating neural systems mediating the acquisition vs. expression of goal-directed and habitual behavioral control. Eur J Neurosci (2015) 41:1358-71. doi:10.1111/ejn.12897
14. Dickinson A. Actions and habits-the development of behavioral autonomy. Philos Trans R Soc Lond B Biol Sci (1985) 308:67-78. doi:10.1098/rstb.1985.0010
15. Balleine BW, Ostlund SB. Still at the choice-point: action selection and initiation in instrumental conditioning. Ann N Y Acad Sci (2007) 1104:147-71. doi:10.1196/annals.1390.006
16. Hammond LJ. The effect of contingency upon the appetitive conditioning of free-operant behavior. J Exp Anal Behav (1980) 34:297-304. doi:10.1901/jeab.1980.34-297
17. Dickinson A, Mulatero CW. Reinforcer specificity of the suppression of instrumental performance on a non-contingent schedule. Behav Processes (1989) 19:167-80. doi:10.1016/0376-6357(89)90039-9
18. Norman DA, Shallice T. Attention to action-willed and automatic-control of behavior. Bull Psychon Soc (1983) 21:354-354.
19. Hogarth L, Balleine BW, Corbit LH, Killcross S. Associative learning mechanisms underpinning the transition from recreational drug use to addiction. Ann N Y Acad Sci (2013) 1282:12-24. doi:10.1111/j.1749-6632.2012.06768.x
20. Miles FJ, Everitt BJ, Dickinson A. Oral cocaine seeking by rats: action or habit? Behav Neurosci (2003) 117:927-38. doi:10.1037/0735-7044.117.5.927
21. Root DH, Fabbricatore AT, Barker DJ, Ma S, Pawlak AP, West MO. Evidence for habitual and goal-directed behavior following devaluation of cocaine: a multifaceted interpretation of relapse. PLoS One (2009) 4:e7170. doi:10.1371/journal.pone.0007170
22. Zapata A, Minney VL, Shippenberg TS. Shift from goal-directed to habitual cocaine seeking after prolonged experience in rats. J Neurosci (2010) 30:15457-63. doi:10.1523/JNEUROSCI.4072-10.2010
23. Corbit LH, Nie H, Janak PH. Habitual alcohol seeking: time course and the contribution of subregions of the dorsal striatum. Biol Psychiatry (2012) 72:389-95. doi:10.1016/j.biopsych.2012.02.024
24. Corbit LH, Nie H, Janak PH. Habitual responding for alcohol depends upon both AMPA and D2 receptor signaling in the dorsolateral striatum. Front Behav Neurosci (2014) 8:301. doi:10.3389/fnbeh.2014.00301
25. Nelson A, Killcross S. Amphetamine exposure enhances habit formation. J Neurosci (2006) 26:3805-12. doi:10.1523/JNEUROSCI.4305-05.2006
26. Nordquist RE, Voorn P, De Mooij-Van Malsen JG, Joosten RN, Pennartz CM, Vanderschuren LJ. Augmented reinforcer value and accelerated habit formation after repeated amphetamine treatment. Eur Neuropsychopharmacol (2007) 17:532-40. doi:10.1016/j.euroneuro.2006.12.005
27. LeBlanc KH, Maidment NT, Ostlund SB. Repeated cocaine exposure facilitates the expression of incentive motivation and induces habitual control in rats. PLoS One (2013) 8:e61355. doi:10.1371/journal.pone.0061355
28. Nelson AJ, Killcross S. Accelerated habit formation following amphetamine exposure is reversed by D1, but enhanced by D2, receptor antagonists. Front Neurosci (2013) 7:76. doi:10.3389/fnins.2013.00076
29. Corbit LH, Chieng BC, Balleine BW. Effects of repeated cocaine exposure on habit learning and reversal by N-acetylcysteine. Neuropsychopharmacology (2014) 39:1893-901. doi:10.1038/npp.2014.37
30. Colwill RM, Rescorla RA. Instrumental responding remains sensitive to reinforcer devaluation after extensive training. J Exp Psychol Anim Behav Process (1985) 11:520-36. doi:10.1037/0097-7403.11.1.120
31. Dickinson A, Smith J, Mirenowicz J. Dissociation of Pavlovian and instrumental incentive learning under dopamine antagonists. Behav Neurosci (2000) 114:468-83. doi:10.1037/0735-7044.114.3.468
32. Colwill RM, Triola SM. Instrumental responding remains under the control of the consequent outcome after extended training. Behav Processes (2002) 57:51-64. doi:10.1016/S0376-6357(01)00204-2
33. Holland PC. Relations between Pavlovian-instrumental transfer and reinforcer devaluation. J Exp Psychol Anim Behav Process (2004) 30:104-17. doi:10.1037/0097-7403.30.2.104
34. Kosaki Y, Dickinson A. Choice and contingency in the development of behavioral autonomy during instrumental conditioning. J Exp Psychol Anim Behav Process (2010) 36:334-42. doi:10.1037/a0016887
35. Daw ND, Niv Y, Dayan P. Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control. Nat Neurosci (2005) 8:1704-11. doi:10.1038/nn1560
36. Wood W, Neal DT. A new look at habits and the habit-goal interface. Psychol Rev (2007) 114:843-63. doi:10.1037/0033-295X.114.4.843
37. LeBlanc KH. A Tale of Two Addiction Theories: The Effects of Cocaine Exposure on Cue-Induced Motivation and Action Control. Los Angeles: University of California (2012).
38. Shiflett MW. The effects of amphetamine exposure on outcome-selective Pavlovian-instrumental transfer in rats. Psychopharmacology (Berl) (2012) 223:361-70. doi:10.1007/s00213-012-2724-y
39. Phillips GD, Vugler A. Effects of sensitization on the detection of an instrumental contingency. Pharmacol Biochem Behav (2011) 100:48-58. doi:10.1016/j.pbb.2011.07.009
40. Son JH, Latimer C, Keefe KA. Impaired formation of stimulus-response, but not action-outcome, associations in rats with methamphetamine-induced neurotoxicity. Neuropsychopharmacology (2011) 36:2441-51. doi:10.1038/npp.2011.131
41. Yin HH, Ostlund SB, Knowlton BJ, Balleine BW. The role of the dorsomedial striatum in instrumental conditioning. Eur J Neurosci (2005) 22:513-23. doi:10.1111/j.1460-9568.2005.04218.x
42. Corbit LH, Ostlund SB, Balleine BW. Sensitivity to instrumental contingency degradation is mediated by the entorhinal cortex and its efferents via the dorsal hippocampus. J Neurosci (2002) 22:10976-84.
43. Braun S, Hauber W. Striatal dopamine depletion in rats produces variable effects on contingency detection: task-related influences. Eur J Neurosci (2012) 35:486-95. doi:10.1111/j.1460-9568.2011.07969.x
44. Colwill RM. Associative representations of instrumental contingencies. Psychol Learn Motiv (1994) 31(31):1-72. doi:10.1016/S0079-7421(08)60408-9
45. Leri F, Stewart J. Drug-induced reinstatement to heroin and cocaine seeking: a rodent model of relapse in polydrug use. Exp Clin Psychopharmacol (2001) 9:297-306. doi:10.1037/1064-1297.9.3.297
46. Delamater AR, Lolordo VM, Sosa W. Outcome-specific conditioned inhibition in Pavlovian backward conditioning. Learn Behav (2003) 31:393-402. doi:10.3758/BF03196000
47. Ostlund SB, Balleine BW. Selective reinstatement of instrumental performance depends on the discriminative stimulus properties of the mediating outcome. Learn Behav (2007) 35:43-52. doi:10.3758/BF03196073
48. Rescorla RA, Skucy JC. Effect of response-independent reinforcers during extinction. J Comp Physiol Psychol (1969) 67:381-9. doi:10.1037/h0026793
49. Corbit LH, Balleine BW. The role of prelimbic cortex in instrumental conditioning. Behav Brain Res (2003) 146:145-57. doi:10.1016/j.bbr.2003.09.023
50. Schmitzer-Torbert N, Apostolidis S, Amoa R, O'Rear C, Kaster M, Stowers J, et al. Post-training cocaine administration facilitates habit learning and requires the infralimbic cortex and dorsolateral striatum. Neurobiol Learn Mem (2015) 118:105-12. doi:10.1016/j.nlm.2014.11.007
51. Schoenbaum G, Setlow B. Cocaine makes actions insensitive to outcomes but not extinction: implications for altered orbitofrontal-amygdalar function. Cereb Cortex (2005) 15:1162-9. doi:10.1093/cercor/bhh216
52. Baker AG, Steinwald H, Bouton ME. Contextual conditioning and reinstatement of extinguished instrumental responding. Q J Exp Psychol B (1991) 43:199-218.
53. Dickinson A, Dawson GR. Pavlovian processes in the motivational control of instrumental performance. Q J Exp Psychol B (1987) 39:201-13.
54. Dickinson A, Dawson GR. The role of the instrumental contingency in the motivational control of performance. Q J Exp Psychol B (1987) 39:77-93.
55. Rescorla RA, Solomon RL. Two-process learning theory: relationships between Pavlovian conditioning and instrumental learning. Psychol Rev (1967) 74:151-82. doi:10.1037/h0024475
56. Jonkman S, Kosaki Y, Everitt BJ, Dickinson A. The role of contextual conditioning in the effect of reinforcer devaluation on instrumental performance by rats. Behav Processes (2010) 83:276-81. doi:10.1016/j.beproc.2009.12.017
57. Killcross S, Coutureau E. Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb Cortex (2003) 13:400-8. doi:10.1093/cercor/13.4.400
58. Pelloux Y, Everitt BJ, Dickinson A. Compulsive drug seeking by rats under punishment: effects of drug taking history. Psychopharmacology (Berl) (2007) 194:127-37. doi:10.1007/s00213-007-0805-0
59. Pelloux Y, Murray JE, Everitt BJ. Differential vulnerability to the punishment of cocaine related behaviours: effects of locus of punishment, cocaine taking history and alternative reinforcer availability. Psychopharmacology (Berl) (2015) 232:125-34. doi:10.1007/s00213-014-3648-5
60. Roesch MR, Takahashi Y, Gugsa N, Bissonette GB, Schoenbaum G. Previous cocaine exposure makes rats hypersensitive to both delay and reward magnitude. J Neurosci (2007) 27:245-50. doi:10.1523/JNEUROSCI.4080-06.2007
61. Ostlund SB, Maidment NT, Balleine BW. Alcohol-paired contextual cues produce an immediate and selective loss of goal-directed action in rats. Front Integr Neurosci (2010) 4:19. doi:10.3389/fnint.2010.00019
62. Furlong TM, Supit AS, Corbit LH, Killcross S, Balleine BW. Pulling habits out of rats: adenosine 2A receptor antagonism in dorsomedial striatum rescues meth-amphetamine-induced deficits in goal-directed action. Addict Biol (2015). doi:10.1111/adb.12316
63. Dickinson A, Charnock DJ. Contingency effects with maintained instrumental reinforcement. Q J Exp Psychol B (1985) 37:397-416.
64. Colwill RM, Rescorla RA. Associative structures in instrumental learning. Psychol Learn Motiv (1986) 20:55-104. doi:10.1016/S0079-7421(08)60016-X
65. Harmer CJ, Phillips GD. Enhanced appetitive conditioning following repeated pretreatment with d-amphetamine. Behav Pharmacol (1998) 9:299-308. doi:10.1097/00008877-199807000-00001
66. Taylor JR, Jentsch JD. Repeated intermittent administration of psychomotor stimulant drugs alters the acquisition of Pavlovian approach behavior in rats: differential effects of cocaine, d-amphetamine and 3, 4-methylenedioxymethamphetamine ("Ecstasy"). Biol Psychiatry (2001) 50:137-43. doi:10.1016/S0006-3223(01)01106-4
67. Wyvell CL, Berridge KC. Incentive sensitization by previous amphetamine exposure: increased cue-triggered "wanting" for sucrose reward. J Neurosci (2001) 21:7831-40.
68. Saddoris MP, Stamatakis A, Carelli RM. Neural correlates of Pavlovian-to-instrumental transfer in the nucleus accumbens shell are selectively potentiated following cocaine self-administration. Eur J Neurosci (2011) 33:2274-87. doi:10.1111/j.1460-9568.2011.07683.x
69. LeBlanc KH, Maidment NT, Ostlund SB. Impact of repeated intravenous cocaine administration on incentive motivation depends on mode of drug delivery. Addict Biol (2014) 19:965-71. doi:10.1111/adb.12063
70. Ostlund SB, Leblanc KH, Kosheleff AR, Wassum KM, Maidment NT. Phasic mesolimbic dopamine signaling encodes the facilitation of incentive motivation produced by repeated cocaine exposure. Neuropsychopharmacology (2014) 39:2441-9. doi:10.1038/npp.2014.96
71. Harmer CJ, Phillips GD. Enhanced dopamine efflux in the amygdala by a predictive, but not a non-predictive, stimulus: facilitation by prior repeated d-amphetamine. Neuroscience (1999) 90:119-30. doi:10.1016/S0306-4522(98)00464-3
72. Lex B, Hauber W. The role of dopamine in the prelimbic cortex and the dorsomedial striatum in instrumental conditioning. Cereb Cortex (2010) 20:873-83. doi:10.1093/cercor/bhp151
73. Wassum KM, Ostlund SB, Balleine BW, Maidment NT. Differential dependence of Pavlovian incentive motivation and instrumental incentive learning processes on dopamine signaling. Learn Mem (2011) 18:475-83. doi:10.1101/lm.2229311
74. Natsheh JY, Shiflett MW. The effects of methylphenidate on goal-directed behavior in a rat model of ADHD. Front Behav Neurosci (2015) 9:326. doi:10.3389/fnbeh.2015.00326
75. Wilens TE, Martelon M, Joshi G, Bateman C, Fried R, Petty C, et al. Does ADHD predict substance-use disorders? A 10-year follow-up study of young adults with ADHD. J Am Acad Child Adolesc Psychiatry (2011) 50:543-53. doi:10.1016/j.jaac.2011.01.021