Abstract
Dual-system theories in psychology and neuroscience propose that a deliberative or goal-directed decision system is accompanied by a more automatic or habitual path to action. In computational terms, the latter is prominently associated with model-free reinforcement learning algorithms such as temporal-difference learning, and the former with model-based approaches. Due in part to the close association between drugs of abuse and dopamine, and also between dopamine, temporal-difference learning, and habitual behavior, addictive drugs are often thought to specifically target the habitual system.
However, although many drug-taking behaviors are well explained under such a theory, evidence suggests that drug-seeking behaviors must leverage a goal-directed controller as well. Indeed, one exhaustive theoretical account proposed that drugs may have numerous, distinct impacts on both systems as well as on other processes.
Here, we seek a more parsimonious account of these phenomena by asking whether the apparent profligacy of drugs’ effects might be explained by a single mechanism of action. In particular, we propose that the pattern of effects observed under drug abuse may reveal interactions between the two controllers, which have typically been modeled as separate and parallel. We sketch several different candidate characterizations and architectures by which model-free effects may impinge on a model-based system, including sharing of cached values through truncated tree search and bias of transition selection for prioritized value sweeping.
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References
Ainslie G (2001) Breakdown of will. Cambridge University Press, Cambridge
Arkadir D, Morris G, Vaadia E, Bergman H (2004) Independent coding of movement direction and reward prediction by single pallidal neurons. J Neurosci 24(45):10047–10056
Balleine BW, Daw ND, O’Doherty JP (2008) Multiple forms of value learning and the function of dopamine. In: Glimcher PW, Camerer CF, Fehr E, Poldrack RA (eds) Neuroeconomics: decision making and the brain. Academic Press, London, pp 367–387
Balleine BW, Delgado MR, Hikosaka O (2007) The role of the dorsal striatum in reward and decision-making. J Neurosci 27(31):8161–8165
Balleine BW, Dickinson A (1998) Goal-directed instrumental action: contingency and incentive learning and their cortical substrates. Neuropharmacology 37(4–5):407–419
Bechara A (2005) Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective. Nat Neurosci 8(11):1458–1463
Berns GS, McClure SM, Pagnoni G, Montague PR (2001) Predictability modulates human brain response to reward. J Neurosci 21(8):2793–2798
Blodgett HC, McCutchan K (1947) Place versus response learning in the simple T-maze. J Exp Psychol 37(5):412–422
Bonson KR, Grant SJ, Contoreggi CS, Links JM, Metcalfe J, Weyl HL et al. (2002) Neural systems and cue-induced cocaine craving. Neuropsychopharmacology 26(3):376–386
Bromberg-Martin ES, Matsumoto M, Hong S, Hikosaka O (2010) A pallidus-habenula-dopamine pathway signals inferred stimulus values. J Neurophysiol 104(2):1068–1076
Buckner RL (2010) The role of the hippocampus in prediction and imagination. Annu Rev Psychol 61:27–48, C1-8
Buckner RL, Carroll DC (2007) Self-projection and the brain. Trends Cogn Sci 11(2):49–57
Carr MF, Jadhav SP, Frank LM (2011) Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nat Neurosci 14(2):147–153
Chib VS, Rangel A, Shimojo S, O’Doherty JP (2009) Evidence for a common representation of decision values for dissimilar goods in human ventromedial prefrontal cortex. J Neurosci 29(39):12315–12320
Davidson TJ, Kloosterman F, Wilson MA (2009) Hippocampal replay of extended experience. Neuron 63(4):497–507
Daw ND, Doya K (2006) The computational neurobiology of learning and reward. Curr Opin Neurobiol 16(2):199–204
Daw ND, Niv Y, Dayan P (2005) Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control. Nat Neurosci 8(12):1704–1711
Daw ND, Gershman SJ, Seymour B, Dayan P, Dolan R (2011) Model-based influences on humans’ choices and striatal prediction errors. Neuron 69(6):1204–1215
Delgado MR, Nystrom LE, Fissell C, Noll DC, Fiez JA (2000) Tracking the hemodynamic responses to reward and punishment in the striatum. J Neurophysiol 84(6):3072–3077
Derdikman D, Moser M-B (2010) A dual role for hippocampal replay. Neuron 65(5):582–584
Di Chiara G (1999) Drug addiction as dopamine-dependent associative learning disorder. Eur J Pharmacol 375(1–3):13–30
Di Ciano P (2008) Facilitated acquisition but not persistence of responding for a cocaine-paired conditioned reinforcer following sensitization with cocaine. Neuropsychopharmacology 33(6):1426–1431
Dickinson A (1985) Actions and habits: The development of behavioural autonomy. Philos Trans R Soc Lond B, Biol Sci 308:67–78
Dickinson A, Balleine B (2002) The role of learning in the operation of motivational systems. In: Stevens’ handbook of experimental psychology. Wiley, New York
Doya K (1999) What are the computations of the cerebellum, the basal ganglia and the cerebral cortex? Neural Netw 12(7–8):961–974
Dragoi G, Tonegawa S (2011) Preplay of future place cell sequences by hippocampal cellular assemblies. Nature 469(7330):397–401
Everitt BJ, Robbins TW (2005) Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 8(11):1481–1489
Everitt BJ, Dickinson A, Robbins TW (2001) The neuropsychological basis of addictive behaviour. Brains Res Rev 36(2–3):129–138
Faure A, Haberland U, Condé F, Massioui NE (2005) Lesion to the nigrostriatal dopamine system disrupts stimulus-response habit formation. J Neurosci 25(11):2771–2780
Foster DJ, Wilson MA (2006) Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440(7084):680–683
Garavan H, Pankiewicz J, Bloom A, Cho JK, Sperry L, Ross TJ et al. (2000) Cue-induced cocaine craving: neuroanatomical specificity for drug users and drug stimuli. Am J Psychiatry 157(11):1789–1798
Gläscher J, Daw ND, Dayan P, O’Doherty JP (2010) States versus rewards: Dissociable neural prediction error signals underlying model-based and model-free reinforcement learning. Neuron 66(4):585–595
Hampton AN, Bossaerts P, O’Doherty JP (2006) The role of the ventromedial prefrontal cortex in abstract state-based inference during decision making in humans. J Neurosci 26(32):8360–8367
Hampton AN, Bossaerts P, O’Doherty JP (2008) Neural correlates of mentalizing-related computations during strategic interactions in humans. Proc Natl Acad Sci 105(18):6741–6746
Hare TA, O’Doherty JP, Camerer CF, Schultz W, Rangel A (2008) Dissociating the role of the orbitofrontal cortex and the striatum in the computation of goal values and prediction errors. J Neurosci 28(22):5623–5630
Hasselmo ME (2008) Temporally structured replay of neural activity in a model of entorhinal cortex, hippocampus and postsubiculum. Eur J Neurosci 28(7):1301–1315
Houk JC, Adams JL, Barto AG (1994) A model of how the basal ganglia generate and use neural signals that predict reinforcement. In: Houk JC, Davis JL, Beiser DG (eds) Models of information processing in the basal ganglia. MIT Press, Cambridge, pp 249–270
Johnson A, Redish AD (2005) Hippocampal replay contributes to within session learning in a temporal difference reinforcement learning model. Neural Netw 18(9):1163–1171
Kable JW, Glimcher PW (2007) The neural correlates of subjective value during intertemporal choice. Nat Neurosci 10(12):1625–1633
Kahneman D, Frederick S (2002) Representativeness revisited: Attribute substitution in intuitive judgment. In: Gilovich T, Griffin DW, Kahneman D (eds) Heuristics and biases: the psychology of intuitive judgement. Cambridge University Press, New York, pp 49–81
Kalivas PW, Volkow ND (2005) The neural basis of addiction: a pathology of motivation and choice. Am J Psychiatry 162(8):1403–1413
Killcross S, Coutureau E (2003) Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb Cortex 13(4):400–408
Kim H, Sul JH, Huh N, Lee D, Jung MW (2009) Role of striatum in updating values of chosen actions. J Neurosci 29(47):14701–14712
Koene RA, Hasselmo ME (2008) Reversed and forward buffering of behavioral spike sequences enables retrospective and prospective retrieval in hippocampal regions CA3 and CA1. Neural Netw 21(2–3):276–288
Lansink CS, Goltstein PM, Lankelma JV, McNaughton BL, Pennartz CMA (2009) Hippocampus leads ventral striatum in replay of place-reward information. PLoS Biol 7(8):e1000173
Loewenstein G, O’Donoghue T (2004) Animal spirits: Affective and deliberative processes in economic behavior (Working Papers Nos. 04–14). Cornell University, Center for Analytic Economics
Lovibond PF (1983) Facilitation of instrumental behavior by a Pavlovian appetitive conditioned stimulus. J Exp Psychol, Anim Behav Processes 9(3):225–247
McClure SM, Berns GS, Montague PR (2003) Temporal prediction errors in a passive learning task activate human striatum. Neuron 38(2):339–346
van der Meer MAA, Johnson A, Schmitzer-Torbert NC, Redish AD (2010) Triple dissociation of information processing in dorsal striatum, ventral striatum, and hippocampus on a learned spatial decision task. Neuron 67(1):25–32
Meil W, See R (1996) Conditioned cued recovery of responding following prolonged withdrawal from self-administered cocaine in rats: an animal model of relapse. Behav Pharmacol 7(8):754–763
Moore AW, Atkeson CG (1993) Prioritized sweeping: Reinforcement learning with less data and less time. Mach Learn 13:103–130. (10.1007/BF00993104)
Nordquist RE, Voorn P, de Mooij-van Malsen JG, Joosten RNJMA, Pennartz CMA, Vanderschuren LJMJ (2007) Augmented reinforcer value and accelerated habit formation after repeated amphetamine treatment. Eur Neuropsychopharmacol 17(8):532–540
O’Doherty JP, Dayan P, Friston K, Critchley H, Dolan RJ (2003) Temporal difference models and reward-related learning in the human brain. Neuron 38(2):329–337
Olmstead MC, Lafond MV, Everitt BJ, Dickinson A (2001) Cocaine seeking by rats is a goal-directed action. Behav Neurosci 115(2):394–402
Pan X, Sawa K, Sakagami M (2007) Model-based reward prediction in the primate prefrontal cortex. Neurosci Res 58(Suppl 1):229
Panlilio LV, Thorndike EB, Schindler CW (2007) Blocking of conditioning to a cocaine-paired stimulus: testing the hypothesis that cocaine perpetually produces a signal of larger-than-expected reward. Pharmacol Biochem Behav 86(4):774–777
Plassmann H, O’Doherty J, Rangel A (2007) Orbitofrontal cortex encodes willingness to pay in everyday economic transactions. J Neurosci 27(37):9984–9988
Poldrack RA, Clark J, Paré-Blagoev EJ, Shohamy D, Creso Moyano J, Myers C et al. (2001) Interactive memory systems in the human brain. Nature 414(6863):546–550
Rangel A, Camerer C, Montague P (2008) A framework for studying the neurobiology of value-based decision making. Nat Rev, Neurosci 9(7):545–556
Redish AD (2004) Addiction as a computational process gone awry. Science 306(5703):1944–1947
Redish AD, Johnson A (2007) A computational model of craving and obsession. Ann NY Acad Sci 1104(1):324–339
Redish AD, Jensen S, Johnson A (2008) Addiction as vulnerabilities in the decision process. Behav Brain Sci 31(04):461–487
Rescorla RA (1994) Control of instrumental performance by Pavlovian and instrumental stimuli. J Exp Psychol, Anim Behav Processes 20(1):44–50
Robinson TE, Berridge KC (2008) The incentive sensitization theory of addiction: some current issues. Philos Trans R Soc Lond B, Biol Sci 363(1507):3137–3146
Root DH, Fabbricatore AT, Barker DJ, Ma S, Pawlak AP, West MO (2009) Evidence for habitual and goal-directed behavior following devaluation of cocaine: a multifaceted interpretation of relapse. PLoS ONE 4(9):e7170
Samejima K, Ueda Y, Doya K, Kimura M (2005) Representation of action-specific reward values in the striatum. Science 310(5752):1337–1340
Schultz W (1998) Predictive reward signal of dopamine neurons. J Neurophysiol 80(1):1–27
Schultz W (2011) Potential vulnerabilities of neuronal reward, risk, and decision mechanisms to addictive drugs. Neuron 69(4):603–617
Schultz W, Dayan P, Montague PR (1997) A neural substrate of prediction and reward. Science 275(5306):1593–1599
See RE (2005) Neural substrates of cocaine-cue associations that trigger relapse. Eur J Pharmacol 526(1–3):140–146
Simon DA, Daw ND (2011) Neural correlates of forward planning in a spatial decision task in humans. J Neurosci 31(14):5526–5539
Sutton RS (1988) Learning to predict by the methods of temporal differences. Mach Learn 3(1):9–44
Sutton RS (1990) Integrated architectures for learning, planning, and reacting based on approximating dynamic programming. In: Proceedings of the seventh International Conference on Machine Learning. Morgan Kaufmann, San Mateo, pp 216–224
Sutton RS, Barto AG (1998) Reinforcement learning. MIT Press, Cambridge
Tanaka SC, Doya K, Okada G, Ueda K, Okamoto Y, Yamawaki S (2004) Prediction of immediate and future rewards differentially recruits cortico-basal ganglia loops. Nat Neurosci 7(8):887–893
Tanaka SC, Samejima K, Okada G, Ueda K, Okamoto Y, Yamawaki S et al. (2006) Brain mechanism of reward prediction under predictable and unpredictable environmental dynamics. Neural Netw 19(8):1233–1241
Thorndike EL (1898) Animal intelligence: An experimental study of the associative processes in animals. Psychol Rev Monogr Suppl 2(4):1–8
Tiffany ST (1990) A cognitive model of drug urges and drug-use behavior: Role of automatic and nonautomatic processes. Psychol Rev 97(2):147–168
Tindell AJ, Smith KS, Berridge KC, Aldridge JW (2009) Dynamic computation of incentive salience: “wanting” what was never “liked”. J Neurosci 29(39):12220–12228
Tolman EC (1948) Cognitive maps in rats and men. Psychol Rev 55:189–208
Tom SM, Fox CR, Trepel C, Poldrack RA (2007) The neural basis of loss aversion in decision-making under risk. Science 315(5811):515–518
Vanderschuren LJMJ, Everitt BJ (2004) Drug seeking becomes compulsive after prolonged cocaine self-administration. Science 305(5686):1017–1019
Verplanken B, Aarts H, van Knippenberg AD, Moonen A (1998) Habit versus planned behaviour: a field experiment. Br J Soc Psychol 37(1):111–128
Volkow ND, Wang G-J, Telang F, Fowler JS, Logan J, Childress A-R et al. (2008) Dopamine increases in striatum do not elicit craving in cocaine abusers unless they are coupled with cocaine cues. NeuroImage 39(3):1266–1273
Wood W, Neal DT (2007) A new look at habits and the habit-goal interface. Psychol Rev 114(4):843–863
Wunderlich K, Rangel A, O’Doherty JP (2009) Neural computations underlying action-based decision making in the human brain. Proc Natl Acad Sci 106(40):17199–17204
Yin HH, Knowlton BJ, Balleine BW (2004) Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur J Neurosci 19(1):181–189
Yin HH, Ostlund SB, Knowlton BJ, Balleine BW (2005) The role of the dorsomedial striatum in instrumental conditioning. Eur J Neurosci 22(2):513–523
Acknowledgements
The authors are supported by a Scholar Award from the McKnight Foundation, a NARSAD Young Investigator Award, Human Frontiers Science Program Grant RGP0036/2009-C, and NIMH grant 1R01MH087882-01, part of the CRCNS program.
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Simon, D.A., Daw, N.D. (2012). Dual-System Learning Models and Drugs of Abuse. In: Gutkin, B., Ahmed, S. (eds) Computational Neuroscience of Drug Addiction. Springer Series in Computational Neuroscience, vol 10. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-0751-5_5
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