Habit, choice, and addiction

Abstract

Addiction was suggested to emerge from the progressive dominance of habits over goal-directed behaviors. However, it is generally assumed that habits do not persist in choice settings. Therefore, it is unclear how drug habits may persist in real-world scenarios where this factor predominates. Here, we discuss the poor translational validity of the habit construct, which impedes our ability to determine its role in addiction. New evidence of habitual behavior in a drug choice setting are then described and discussed. Interestingly, habitual preference did not promote drug choice but instead favored abstinence. Here, we propose several clues to reconcile these unexpected results with the habit theory of addiction, and we highlight the need in experimental research to face the complexity of drug addicts’ decision-making environments by investigating drug habits in the context of choice and in the presence of cues. On a theoretical level, we need to consider more complex frameworks, taking into account continuous interactions between goal-directed and habitual systems, and alternative decision-making models more representative of real-world conditions.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Habitual preference for saccharin in a drug choice setting.
Fig. 2: Inflexible preference for the alternative nondrug reward in a drug choice setting is under habitual, model-free control.
Fig. 3: Rats are oblivious to the cocaine option during self-initiated choice.

References

  1. 1.

    Redish AD, Jensen S, Johnson A. A unified framework for addiction: vulnerabilities in the decision process. Behav Brain Sci. 2008;31:415–87.

    Article  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Everitt BJ, Robbins TW. Drug addiction: updating actions to habits to compulsions ten years on. Annu Rev Psychol. 2016;67:23–50.

    Article  PubMed  Google Scholar 

  3. 3.

    Everitt BJ, Robbins TW. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci. 2005;8:1481–9.

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    Tiffany ST. A cognitive model of drug urges and drug-use behavior: role of automatic and nonautomatic processes. Psychol Rev. 1990;97:147–68.

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    Heather N. Is the concept of compulsion useful in the explanation or description of addictive behaviour and experience? Addict Behav Rep. 2017;6:15–38.

    PubMed  PubMed Central  Google Scholar 

  6. 6.

    Ostlund SB, Balleine BW. On habits and addiction: an associative analysis of compulsive drug seeking. Drug Discov Today Dis Model 2008;5:235–45.

    Article  Google Scholar 

  7. 7.

    Dickinson A, Balleine B. Motivational control of instrumental action. Anim Learn Behav. 1994;22:1–18.

    Article  Google Scholar 

  8. 8.

    Balleine BW, Dickinson A. Goal-directed instrumental action: contingency and incentive learning and their cortical substrates. Neuropharmacology. 1998;37:407–19.

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Hogarth L, Lam-Cassettari C, Pacitti H, Currah T, Mahlberg J, Hartley L, et al. Intact goal-directed control in treatment-seeking drug users indexed by outcome-devaluation and Pavlovian to instrumental transfer: critique of habit theory. Eur J Neurosci. 2018;50:2513–2525.

  10. 10.

    Hogarth L. Addiction is driven by excessive goal-directed drug choice under negative affect: translational critique of habit and compulsion theory. Neuropsychopharmacology. 2020;45:720–735. https://doi.org/10.1038/s41386-020-0600-8.

  11. 11.

    Corbit L, Nie H, Janak P. Habitual alcohol seeking: time course and the contribution of subregions of the dorsal striatum. Biol Psychiatry. 2012;72:389–95.

    Article  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Barker JM, Zhang H, Villafane JJ, Wang TL, Torregrossa MM, Taylor JR. Epigenetic and pharmacological regulation of 5HT3 receptors controls compulsive ethanol seeking in mice. Eur J Neurosci. 2014;39:999–1008.

    Article  PubMed  PubMed Central  Google Scholar 

  13. 13.

    Dickinson A, Wood N, Smith JW. Alcohol seeking by rats: action or habit? Q J Exp Psychol B 2002;55:331–48.

    Article  PubMed  Google Scholar 

  14. 14.

    Lopez MF, Becker HC, Chandler LJ. Repeated episodes of chronic intermittent ethanol promote insensitivity to devaluation of the reinforcing effect of ethanol. Alcohol. 2014;48:639–45.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. 15.

    Mangieri RA, Cofresí RU, Gonzales RA. Ethanol seeking by long evans rats is not always a goal-directed behavior. PLoS ONE. 2012;7:1–13.

    Article  CAS  Google Scholar 

  16. 16.

    Mangieri RA, Cofresí RU, Gonzales RA. Ethanol exposure interacts with training conditions to influence behavioral adaptation to a negative instrumental contingency. Front Behav Neurosci. 2014;8:220.

    Article  PubMed  PubMed Central  Google Scholar 

  17. 17.

    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;8:1–9.

    Article  CAS  Google Scholar 

  18. 18.

    Miles FJ, Everitt BJ, Dickinson A. Oral cocaine seeking by rats: action or habit? Behav Neurosci. 2003;117:927–38.

    Article  PubMed  Google Scholar 

  19. 19.

    Leong KC, Berini CR, Ghee SM, Reichel CM. Extended cocaine-seeking produces a shift from goal-directed to habitual responding in rats. Physiol Behav. 2016;164:330–5.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Clemens KJ, Lay BP, Holmes NM. Extended nicotine self-administration increases sensitivity to nicotine, motivation to seek nicotine and the reinforcing properties of nicotine-paired cues. Addict Biol. 2015;22:400–410.

    Article  CAS  PubMed  Google Scholar 

  21. 21.

    Loughlin A, Funk D, Coen K, Lê AD. Habitual nicotine-seeking in rats following limited training. Psychopharmacology. 2017;234:2619–2629.

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Olmstead MC, Lafonda MV, Everittb BJ, Dickinsonb A. Cocaine seeking by rats is a goal-directed action. Behav Neurosci. 2001;115:394–402.

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Hutcheson DM, Everitt BJ, Robbins TW, Dickinson A. The role of withdrawal in heroin addiction: enhances reward or promotes avoidance? Nat Neurosci. 2001;4:943–7.

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    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.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Renteria R, Baltz ET, Gremel CM. Chronic alcohol exposure disrupts top-down control over basal ganglia action selection to produce habits. Nat Commun. 2018;9:1–11.

    CAS  Article  Google Scholar 

  26. 26.

    Corbit LH, Chieng BC, Balleine BW. Effects of repeated cocaine exposure on habit learning and reversal by N-acetylcysteine. Neuropsychopharmacology. 2014;39:1893–901.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. 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:e61355:1-10.

  28. 28.

    Nelson A, Killcross S. Amphetamine exposure enhances habit formation. J Neurosci. 2006;26:3805–12.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. 29.

    Nordquist RE, Voorn P, de Mooij-van Malsen JG, Joosten RNJMA, Pennartz CMA, Vanderschuren LJMJ. Augmented reinforcer value and accelerated habit formation after repeated amphetamine treatment. Eur Neuropsychopharmacol. 2007;17:532–40.

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Nelson AJD, Killcross S, Leblanc KH. Accelerated habit formation following amphetamine exposure is reversed by D 1, but enhanced by D 2, receptor antagonists. Front Neurosci. 2013;7:1–13.

    Article  Google Scholar 

  31. 31.

    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.

    CAS  Article  Google Scholar 

  32. 32.

    Shiflett MW. The effects of amphetamine exposure on outcome-selective Pavlovian-instrumental transfer in rats. Psychopharmacology. 2012;223:361–70.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Gourley SL, Olevska A, Gordon J, Taylor JR. Cytoskeletal determinants of stimulus-response habits. J Neurosci. 2013;33:11811–6.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Halbout B, Liu AT, Ostlund SB. A closer look at the effects of repeated cocaine exposure on adaptive decision-making under conditions that promote goal-directed control. Front Psychiatry. 2016;7:1–12.

    Article  Google Scholar 

  35. 35.

    Phillips GD, Vugler A. Effects of sensitization on the detection of an instrumental contingency. Pharmacol Biochem Behav. 2011;100:48–58.

    CAS  Article  Google Scholar 

  36. 36.

    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.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Dickinson A, Nicholas DJ, Adams CD. The effect of the instrumental training contingency on susceptibility to reinforcer devaluation. Q J Exp Psychol Sect B. 1983;35:35–51.

    Article  Google Scholar 

  38. 38.

    Derusso AL, Fan D, Gupta J, Shelest O, Costa RM, Yin HH. Instrumental uncertainty as a determinant of behavior under interval schedules of reinforcement. Front Integr Neurosci. 2010;4:1–8.

    Article  Google Scholar 

  39. 39.

    Urcelay GP, Jonkman S. Delayed rewards facilitate habit formation delayed rewards facilitate habit formation. J Exp Psychol Anim Learn Cogn. 2019;45:413–421.

    Article  Google Scholar 

  40. 40.

    Adams CD. Variations in the sensitivity of instrumental responding to reinforcer devaluation. Q J Exp Psychol Sect B. 1982;34:77–98.

    Article  Google Scholar 

  41. 41.

    Dickinson A. Actions and habits: the development of behavioural autonomy. Philos Trans R Soc B Biol Sci. 1985;308:67–78.

    Google Scholar 

  42. 42.

    Holland PC. Relations between Pavlovian-instrumental transfer and reinforcer devaluation. J Exp Psychol Anim Behav Process. 2004;30:104–17.

    Article  Google Scholar 

  43. 43.

    Colwill RM, Triola SM. Instrumental responding remains under the control of the consequent outcome after extended training. Behav Process. 2002;57:51–64.

    Article  Google Scholar 

  44. 44.

    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.

    Article  Google Scholar 

  45. 45.

    Trask S, Shipman ML, Green JT, Bouton ME. Some factors that restore goal-direction to a habitual behavior. Neurobiol Learn Mem. 2020;169:107161.

  46. 46.

    Bouton ME, Broomer MC, Rey CN, Thrailkill EA. Unexpected food outcomes can return a habit to goal-directed action. Neurobiol Learn Mem. 2020;169:1–9.

    Article  Google Scholar 

  47. 47.

    Thrailkill EA, Trask S, Vidal P, Alcalá JA, Bouton ME. Stimulus control of actions and habits: a role for reinforcer predictability and attention in the development of habitual behavior. J Exp Psychol Anim Learn Cogn. 2018;44:370–84.

    Article  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Dolan RJ, Dayan P. Goals and habits in the brain. Neuron. 2013;80:312–25.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  49. 49.

    Keramati M, Smittenaar P, Dolan RJ, Dayan P. Adaptive integration of habits into depth-limited planning defines a habitual-goal-directed spectrum. Proc Natl Acad Sci USA. 2016;113:12868–73.

    CAS  Article  Google Scholar 

  50. 50.

    Vandaele Y, Guillem K, Ahmed SH, Ahmed SH. Habitual preference for the nondrug reward in a drug choice setting. Front Behav Neurosci. 2020;14:1–9.

    Article  Google Scholar 

  51. 51.

    Vandaele Y, Vouillac-Mendoza C, Ahmed SH. Inflexible habitual decision-making during choice between cocaine and a nondrug alternative. Transl Psychiatry. 2019;9:109.

  52. 52.

    Daw ND, Niv Y, Dayan P. Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control. Nat Neurosci. 2005;8:1704–11.

    CAS  Article  PubMed  Google Scholar 

  53. 53.

    Daw ND, Gershman SJ, Seymour B, Dayan P, Dolan RJ. Model-based influences on humans’ choices and striatal prediction errors. Neuron. 2011;69:1204–15.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Doya K, Samejima K, Katagiri K, Kawato M. Multiple model-based reinforcement learning. Neural Comput. 2002;14:1347–69.

    Article  PubMed  Google Scholar 

  55. 55.

    Vandaele Y, Pribut HJ, Janak PH. Lever insertion as a salient stimulus promoting insensitivity to outcome devaluation. Front Integr Neurosci. 2017;11:1–13.

    Article  CAS  Google Scholar 

  56. 56.

    Vandaele Y, Mahajan NR, Ottenheimer DJ, Richard JM, Mysore SP, Janak PH. Distinct recruitment of dorsomedial and dorsolateral striatum erodes with extended training. Elife. 2019;8:1–29.

    Article  Google Scholar 

  57. 57.

    Lee SW, Shimojo S, O’Doherty JP. Neural computations underlying arbitration between model-based and model-free learning. Neuron. 2014;81:687–99.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  58. 58.

    Colwill RM, Rescorla RA. Instrumental responding remains sensitive to reinforcer devaluation after extensive training. J Exp Psychol Anim Behav Process. 1985;11:520–36.

    Article  Google Scholar 

  59. 59.

    Parkes SL, Balleine BW. Incentive memory: evidence the basolateral amygdala encodes and the insular cortex retrieves outcome values to guide choice between goal-directed actions. J Neurosci. 2013;33:8753–63.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  60. 60.

    Parkes SL, Bradfield LA, Balleine BW. Interaction of insular cortex and ventral striatum mediates the effect of incentive memory on choice between goal-directed actions. J Neurosci. 2015;35:6464–71.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  61. 61.

    Balleine BW, Killcross AS, Dickinson A. The effect oflesions ofthe basolateral amygdala on instrumental conditioning. J Neurosci. 2003;23:666–75.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  62. 62.

    Corbit LH, Balleine BW. The role of prelimbic cortex in instrumental conditioning. Behav Brain Res. 2003;146:145–57.

    Article  PubMed  Google Scholar 

  63. 63.

    Glimcher PW, Rustichini A. Neuroeconomics: the consilience of brain and decision. Science. 2004;306:447–52.

    CAS  Article  PubMed  Google Scholar 

  64. 64.

    Rangel A, Camerer C, Montague PR. A framework for studying the neurobiology of value-based decision making. Nat Rev Neurosci. 2008;9:545–56.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  65. 65.

    Rushworth MF, Mars RB, Summerfield C. General mechanisms for making decisions? Curr Opin Neurobiol. 2009;19:75–83.

    CAS  Article  PubMed  Google Scholar 

  66. 66.

    Rangel A, Hare T. Neural computations associated with goal-directed choice. Curr Opin Neurobiol. 2010;20:262–70.

    CAS  Article  PubMed  Google Scholar 

  67. 67.

    Keramati M, Dezfouli A, Piray P. Speed/accuracy trade-off between the habitual and the goal-directed processes. PLoS Comput Biol. 2011;7:e1002055.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  68. 68.

    Lenoir M, Augier E, Vouillac C, Ahmed SH. A choice-based screening method for compulsive drug users in rats. Curr Protoc Neurosci. 2013;1:1–17.

    Google Scholar 

  69. 69.

    Cantin L, Lenoir M, Augier E, Vanhille N, Dubreucq S, Serre F, et al. Cocaine is low on the value ladder of rats: Possible evidence for resilience to addiction. PLoS ONE. 2010;5:e11592:1–14.

  70. 70.

    Lenoir M, Serre F, Cantin L, Ahmed SH. Intense sweetness surpasses cocaine reward. PLoS ONE. 2007;2:e698:1–10.

  71. 71.

    Ahmed SH. The science of making drug-addicted animals. Neuroscience. 2012;211:107–25.

    CAS  Article  PubMed  Google Scholar 

  72. 72.

    Namba MD, Tomek SE, Olive MF, Beckmann JS, Gipson CD. The winding road to relapse: forging a new understanding of cue-induced reinstatement models and their associated neural mechanisms. Front Behav Neurosci. 2018;12:1–22.

    Article  CAS  Google Scholar 

  73. 73.

    Weiss F, Maldonado-Vlaar CS, Parsons LH, Kerr TM, Smith DL, Ben-Shahar O. Control of cocaine-seeking behavior by drug-associated stimuli in rats: Effects on recovery of extinguished operant-responding and extracellular dopamine levels in amygdala and nucleus accumbens. Proc Natl Acad Sci USA. 2000;97:4321–6.

    CAS  Article  PubMed  Google Scholar 

  74. 74.

    Weiss F, Martin-Fardon R, Ciccocioppo R, Kerr TM, Smith DL, Ben-Shahar O. Enduring resistance to extinction of cocaine-seeking behavior induced by drug-related cues. Neuropsychopharmacology. 2001;25:361–72.

    CAS  Article  PubMed  Google Scholar 

  75. 75.

    Shaham Y, Shalev U, Lu L, de Wit H, Stewart J. The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology. 2003;168:3–20.

    CAS  Article  PubMed  Google Scholar 

  76. 76.

    Crombag HS, Bossert JM, Koya E, Shaham Y. Context-induced relapse to drug seeking: a review. Philos Trans R Soc B Biol Sci. 2008;363:3233–43.

    Article  Google Scholar 

  77. 77.

    Hogarth L, Chase HW. Parallel goal-directed and habitual control of human drug-seeking: implications for dependence vulnerability. J Exp Psychol Anim Behav Process. 2011;37:261–76.

    Article  PubMed  Google Scholar 

  78. 78.

    Hogarth L. Goal-directed and transfer-cue-elicited drug-seeking are dissociated by pharmacotherapy: evidence for independent additive controllers. J Exp Psychol Anim Behav Process. 2012;38:266–78.

    Article  PubMed  Google Scholar 

  79. 79.

    Corbit LH, Janak PH, Balleine BW. General and outcome-specific forms of Pavlovian-instrumental transfer: the effect of shifts in motivational state and inactivation of the ventral tegmental area. Eur J Neurosci. 2007;26:3141–9.

    Article  PubMed  Google Scholar 

  80. 80.

    Rescorla RA. Transfer of instrumental control mediated by a devalued outcome. Anim Learn Behav. 1994;22:27–33.

    Article  Google Scholar 

  81. 81.

    Watson P, Wiers RW, Hommel B, de Wit S. Working for food you don’t desire. Cues interfere with goal-directed food-seeking. Appetite 2014;79:139–48.

    CAS  Article  PubMed  Google Scholar 

  82. 82.

    Van Steenbergen H, Watson P, Wiers RW, Hommel B, de Wit S. Dissociable corticostriatal circuits underlie goal-directed vs. cue-elicited habitual food seeking after satiation: evidence from a multimodal MRI study. Eur J Neurosci. 2017;46:1815–1827.

    Article  PubMed  Google Scholar 

  83. 83.

    Lamb RJ, Schindler W, Pinkston JW. Conditioned stimuli’s role in relapse: pre-clinical research on pavlovian instrumental transfer. Psychopharmacology. 2016;233:1933–44.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  84. 84.

    Kelleher RT, Gollub LR. A review of positive conditioned reinforcement. J Exp Anal Behav. 1962;5:543–97.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  85. 85.

    Bossert JM, Marchant NJ, Calu DJ, Shaham Y. The reinstatement model of drug relapse: recent neurobiological findings, emerging research topics, and translational research. Psychopharmacology. 2013;229:453–76.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  86. 86.

    Hu Y, Salmeron BJ, Krasnova IN, Gu H, Lu H, Bonci A, et al. Compulsive drug use is associated with imbalance of orbitofrontal- And prelimbic-striatal circuits in punishment-resistant individuals. Proc Natl Acad Sci USA. 2019;116:9066–71.

    CAS  Article  PubMed  Google Scholar 

  87. 87.

    Pascoli V, Terrier J, Hiver A, Lüscher C. Sufficiency of mesolimbic dopamine neuron stimulation for the progression to addiction. Neuron. 2015;88:1054–66.

    CAS  Article  PubMed  Google Scholar 

  88. 88.

    Pascoli V, Hiver A, Van Zessen R, Loureiro M, Achargui R, Harada M, et al. Stochastic synaptic plasticity underlying compulsion in a model of addiction. Nature. 2018;564:366–71.

    CAS  Article  PubMed  Google Scholar 

  89. 89.

    Lüscher C, Robbins TW, Everitt BJ. The transition to compulsion in addiction. Nat Rev Neurosci. 2020;21:247–63.

    Article  CAS  PubMed  Google Scholar 

  90. 90.

    Goldstein RZ, Volkow ND. Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nat Rev Neurosci. 2012;12:652–69.

    Article  CAS  Google Scholar 

  91. 91.

    Baler RD, Volkow ND. Drug addiction: the neurobiology of disrupted self-control. Trends Mol Med. 2006;12:559–66.

    CAS  Article  PubMed  Google Scholar 

  92. 92.

    Belin D, Everitt BJ. Cocaine seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum. Neuron. 2008;57:432–41.

    CAS  Article  PubMed  Google Scholar 

  93. 93.

    Willuhn I, Burgeno LM, Everitt BJ, Phillips PEM. Hierarchical recruitment of phasic dopamine signaling in the striatum during the progression of cocaine use. Proc Natl Acad Sci USA. 2012;109:20703–8.

    CAS  Article  PubMed  Google Scholar 

  94. 94.

    Yin HH, Ostlund SB, Knowlton BJ, Balleine BW. The role of the dorsomedial striatum in instrumental conditioning. Eur J Neurosci. 2005;22:513–23.

    Article  PubMed  Google Scholar 

  95. 95.

    Yin HH, Knowlton BJ, Balleine BW. Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur J Neurosci. 2004;19:181–9.

    Article  PubMed  Google Scholar 

  96. 96.

    Yin HH, Knowlton BJ. The role of the basal ganglia in habit formation. Nat Rev Neurosci. 2006;7:464–76.

    CAS  Article  PubMed  Google Scholar 

  97. 97.

    Balleine BW, Liljeholm M, Ostlund SB. The integrative function of the basal ganglia in instrumental conditioning. Behav Brain Res. 2009;199:43–52.

    Article  PubMed  Google Scholar 

  98. 98.

    Murray JE, Belin D, Everitt BJ. Double dissociation of the dorsomedial and dorsolateral striatal control over the acquisition and performance of cocaine seeking. Neuropsychopharmacology. 2012;37:2456–66.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  99. 99.

    Preble E. Taking care of business—the heroin user’ s life on the street. Int J Addict. 1969;4:1–24.

    Article  Google Scholar 

  100. 100.

    Schreiner DC, Renteria R, Gremel CM. Fractionating the all-or-nothing definition of goal-directed and habitual decision-making. J Neurosci Res. 2019;98:998–1006.

    Article  CAS  PubMed  Google Scholar 

  101. 101.

    Feher da Silva C, Hare TA. Humans primarily use model-based inference in the two-stage task. Nat Hum Behav. 2020. https://doi.org/10.1038/s41562-020-0905-y.

    Article  PubMed  Google Scholar 

  102. 102.

    Byrne KA, Otto AR, Pang B, Patrick CJ, Worthy DA. Substance use is associated with reduced devaluation sensitivity. Cogn Affect Behav Neurosci. 2019;19:40–55.

    Article  PubMed  Google Scholar 

  103. 103.

    Gillan CM, Kosinski M, Whelan R, Phelps EA, Daw ND. Characterizing a psychiatric symptom dimension related to deficits in goal-directed control. Elife. 2016;5:e11305:1–24.

  104. 104.

    Miller KJ, Botvinick MM, Brody CD. Dorsal hippocampus contributes to model-based planning. Nat Neurosci. 2017;20:1269–76.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  105. 105.

    Groman SM, Massi B, Mathias SR, Lee D, Taylor JR. Model-free and model-based influences in addiction-related behaviors. Biol Psychiatry. 2019;85:936–45.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  106. 106.

    Groman SM, Massi B, Mathias SR, Curry DW, Lee D, Taylor JR. Neurochemical and behavioral dissections of decision-making in a rodent multistage task. J Neurosci. 2019;39:295–306.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  107. 107.

    Fraser KM, Janak PH. How does drug use shift the balance between model-based and model-free control of decision making? Biol Psychiatry. 2019;85:886–8.

    Article  PubMed  Google Scholar 

  108. 108.

    Otto AR, Gershman SJ, Markman AB, Daw ND. The curse of planning. Psychol Sci. 2013;24:751–61.

    Article  PubMed  Google Scholar 

  109. 109.

    Dezfouli A, Balleine BW. Actions, action sequences and habits: evidence that goal-directed and habitual action control are hierarchically organized. PLoS Comput Biol. 2013;9:e1003364.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. 110.

    Dezfouli A, Balleine BW. Habits, action sequences and reinforcement learning. Eur J Neurosci. 2012;35:1036–51. https://doi.org/10.1038/s41386-020-0600-8.

  111. 111.

    Dezfouli A, Lingawi NW, Balleine BW. Habits as action sequences: hierarchical action control and changes in outcome value. Philos Trans R Soc L B Biol Sci. 2014;369:20130482.

  112. 112.

    Balleine BW, Dezfouli A. Hierarchical action control: adaptive collaboration between actions and habits. Front Psychol. 2019;10:1–13.

    Article  Google Scholar 

  113. 113.

    Cushman F, Morris A. Habitual control of goal selection in humans. Proc Natl Acad Sci USA. 2015;112:13817–22.

    CAS  Article  PubMed  Google Scholar 

  114. 114.

    Wood W, Neal DT. A new look at habits and the habit—goal interface. Psychol Rev. 2007;114:843–63.

    Article  PubMed  Google Scholar 

  115. 115.

    Kruglanski AW, Szumowska E. Habitual behavior is goal-driven. Perspect Psychol Sci. 2020. https://doi.org/10.1177/1745691620917676.

  116. 116.

    Huys QJM, Eshel N, O’Nions E, Sheridan L, Dayan P, Roiser JP. Bonsai trees in your head: how the pavlovian system sculpts goal-directed choices by pruning decision trees. PLoS Comput Biol. 2012;8:1–13.

    Article  CAS  Google Scholar 

  117. 117.

    Vandaele Y, Vouillac-Mendoza C, Ahmed SH. Cocaine falls into oblivion during volitional initiation of choice trials. Addict Biol. 2020. In press.

  118. 118.

    Shapiro MS, Siller S, Kacelnik A. 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). J Exp Psychol Anim Behav Process. 2008;34:75–93.

    Article  PubMed  Google Scholar 

  119. 119.

    Freidin E, Aw J, Kacelnik A. Sequential and simultaneous choices: testing the diet selection and sequential choice models. Behav Process. 2009;80:218–23.

    Article  Google Scholar 

  120. 120.

    Freidin E, Kacelnik A. Rational choice, context dependence, and the value of information in European starlings (Sturnus vulgaris). Science. 2011;334:1000–2.

    CAS  Article  PubMed  Google Scholar 

  121. 121.

    Vasconcelos M, Monteiro T, Aw J, Kacelnik A. Choice in multi-alternative environments: a trial-by-trial implementation of the sequential choice model. Behav Process. 2010;84:435–9.

    Article  Google Scholar 

  122. 122.

    Vasconcelos M, Monteiro T, Kacelnik A. Context-dependent preferences in starlings: linking ecology, foraging and choice. PLoS ONE. 2013;8:1–8.

    Article  Google Scholar 

  123. 123.

    Mobbs D, Trimmer PC, Blumstein DT, Dayan P. Foraging for foundations in decision neuroscience: insights from ethology. Nat Rev Neurosci. 2018;19:419–27.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  124. 124.

    Grace RC. Acquisition of choice in concurrent chains: assessing the cumulative decision model. Behav Process. 2016;126:82–93.

    Article  Google Scholar 

  125. 125.

    Singer BF, Fadanelli M, Kawa AB, Robinson TE. Are cocaine-seeking “ habits” necessary for the development of addiction-like behavior in rats? J Neurosci. 2017;38:60–73.

    Article  PubMed  Google Scholar 

  126. 126.

    Colwill RM. An associative analysis of instrumental learning. Curr Dir Psychol Sci. 1993;2:111–6.

    Article  Google Scholar 

  127. 127.

    Dickinson A, Mulatero CW. Reinforcer specificity of the suppression of instrumental performance on a non-contingent schedule. Behav Processes. 1989;19:167–80.

    CAS  Article  PubMed  Google Scholar 

  128. 128.

    Rescorla RA. A Pavlovian analysis of goal-directed behavior. American Psychologist 1987;42:119–29.

    Article  Google Scholar 

  129. 129.

    Adams CD, Dickinson A. Instrumental responding following reinforcer devaluation. Q J Exp Psychol Sect B Comp Physiol Psychol. 1981;33:109–121.

  130. 130.

    Gläscher J, Daw N, Dayan P, O'Doherty JP. States versus Rewards: Dissociable Neural Prediction Error Signals Underlying Model-Based and Model-Free Reinforcement Learning. Neuron 2010;66:585–95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Christophe Bernard, Mathieu Louvet, and Eric Wattelet for administrative assistance. We also thank Dr. Patricia Janak for her helpful comments on a previous version of the review, and Emma Chaloux-Pinette for proofreading the paper.

Author information

Affiliations

Authors

Contributions

YV drafted the first version of the paper; SHA and YV revised and edited the paper; YV and SHA approved the final version of the paper.

Corresponding author

Correspondence to Y. Vandaele.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Vandaele, Y., Ahmed, S.H. Habit, choice, and addiction. Neuropsychopharmacol. (2020). https://doi.org/10.1038/s41386-020-00899-y

Download citation

Search