Skip to main content

Computational Models of Incentive-Sensitization in Addiction: Dynamic Limbic Transformation of Learning into Motivation

  • Chapter
Computational Neuroscience of Drug Addiction

Part of the book series: Springer Series in Computational Neuroscience ((NEUROSCI,volume 10))

Abstract

Incentive salience is a motivational magnet property attributed to reward-predicting conditioned stimuli (cues). This property makes the cue and its associated unconditioned reward ‘wanted’ at that moment, and pulls an individual’s behavior towards those stimuli. The incentive-sensitization theory of addiction posits that permanent changes in brain mesolimbic systems in drug addicts can amplify the incentive salience of Pavlovian drug cues to produce excessive ‘wanting’ to take drugs. Similarly, drug intoxication and natural appetite states can temporarily and dynamically amplify cue-triggered ‘wanting’, promoting binge consumption. Finally, sensitization and drug intoxication can add synergistically to produce especially strong moments of urge for reward. Here we describe a computational model of incentive salience that captures all these properties, and contrast it to traditional cache-based models of reinforcement and reward learning. Our motivation-based model incorporates dynamically modulated physiological brain states that change the ability of cues to elicit ‘wanting’ on the fly. These brain states include the presence of a drug of abuse and longer-term mesolimbic sensitization, both of which boost mesocorticolimbic cue-triggered signals. We have tested our model by recording neuronal activity from mesolimbic output signals for reward and Pavlovian cues in the ventral pallidum (VP), and a novel technique for analyzing neuronal firing “profile”, presents evidence in support of our dynamic motivational account of incentive salience.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Berridge KC (2001) Reward learning: Reinforcement, incentives, and expectations. In: Medin DL (ed) The psychology of learning and motivation, vol 40. Academic Press, New York, pp 223–278

    Google Scholar 

  • Berridge KC (2004) Motivational concepts in behavioral neuroscience. Physiol Behav 81:179–209

    Article  PubMed  CAS  Google Scholar 

  • Berridge KC (2007) The debate over dopamine in reward: the case for incentive salience. Psychopharmacology 191:391–431 (2007)

    Article  PubMed  CAS  Google Scholar 

  • Berridge KC, Aldridge JW (2008) Decision utility, the brain, and pursuit of hedonic goals. Social Cogn 26:621–646

    Article  Google Scholar 

  • Berridge KC, Robinson TE (1998) What is the role of dopamine in reward: hedonic impact, reward learning, and incentive salience? Brains Res Rev 28:309–369

    Article  CAS  Google Scholar 

  • Berridge KC, Robinson TE (2003) Parsing reward. Trends Neurosci 26:507–513

    Article  PubMed  CAS  Google Scholar 

  • Berridge KC, Valenstein ES (1991) What psychological process mediates feeding evoked by electrical stimulation of the lateral hypothalamus? Behav Neurosci 105:3–14

    Article  PubMed  CAS  Google Scholar 

  • Bindra D (1978) How adaptive behavior is produced: a perceptual-motivation alternative to response reinforcement. Behav Brain Sci 1:41–91

    Article  Google Scholar 

  • Daw ND, Niv Y, Dayan P (2005a) Uncertainty-based competition between prefrontal and dorsal striatal systems of behavioral control. Nat Neurosci 8:1704–1711

    Article  PubMed  CAS  Google Scholar 

  • Daw ND, Niv Y, Dayan P (2005b) Actions, policies, values, and the basal ganglia. In: Bezard (ed) Recent breakthroughs in basal ganglia research. Nova Publ, New York, pp 91–106

    Google Scholar 

  • Dayan P (2009) Dopamine, reinforcement learning, and addiction. Pharmacopsychiatry 42(S 01):S56–S65

    Article  PubMed  Google Scholar 

  • Dayan P, Balleine BW (2002) Reward, motivation and reinforcement learning. Neuron 36:285–298

    Article  PubMed  CAS  Google Scholar 

  • Dickinson A, Balleine B (2002) The role of learning in the operation of motivational systems. In: Gallistel CR (ed) Stevens’ handbook of experimental psychology: learning, motivation, and emotion, vol 3, 3rd edn. Wiley, New York, pp 497–534

    Google Scholar 

  • Frederick S, Loewenstein G, O’Donoghue T (2002) Time discounting and time preference: A critical review. J Econ Lit 40:351–401

    Article  Google Scholar 

  • Giordano LA, Bickel WK, Loewenstein G, Jacobs EA, Marsch L, Badger GJ (2002) Mild opioid deprivation increases the degree that opioid-dependent outpatients discount delayed heroin and money. Psychopharmacology 163:174–182

    Article  PubMed  CAS  Google Scholar 

  • Glimcher PW, Kable O (2005) Neural mechanisms of temporal discounting in humans. Abstract for 2005 annual meeting of the society for neuroeconomics

    Google Scholar 

  • Gong W, Neill D, Justice JB Jr (1996) Conditioned place preference and locomotor activation produced by injection of psychostimulants into ventral pallidum. Brain Res 707(1):64–74

    Article  PubMed  CAS  Google Scholar 

  • Gutkin BS, Dehaene S, Changeux JP (2006) A neurocomputational hypothesis for nicotine addiction. Proc Natl Acad Sci USA 103(4):1106–1111

    Article  PubMed  CAS  Google Scholar 

  • Koob GF, Le Moal M (2006) Neurobiology of addiction. Academic Press, New York

    Google Scholar 

  • Laibson D (1997) Golden eggs and hyperbolic discounting. Q J Econ 112(2):443–477

    Article  Google Scholar 

  • Louie K, Glimcher PW (2005) Intertemporal choice behavior in monkeys: interaction between delay to reward, subjective value, and area LP. Abstract for 2005 annual meeting of the society for neuroeconomics

    Google Scholar 

  • McClure SM, Daw ND, Montague PR (2003) A computational substrate for incentive salience. Trends Neurosci 26:423–428

    Article  PubMed  CAS  Google Scholar 

  • McClure SM, Laibson DI, Loewenstein G, Cohen JD (2004) Separate neural systems value immediate and delayed monetary rewards. Science 306:503–507

    Article  PubMed  CAS  Google Scholar 

  • McFarland K, Davidge SB, Lapish CC, Kalivas PW (2004) Limbic and motor circuitry underlying footshock-induced reinstatement of cocaine-seeking behavior. J Neurosci 24(7):1551–1560

    Article  PubMed  CAS  Google Scholar 

  • Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–202

    Article  PubMed  CAS  Google Scholar 

  • Montague PR, Hyman SE, Cohen JD (2004) Computational roles for dopamine in behavioral control. Nature 760–767

    Google Scholar 

  • Niv Y, Joel D, Dayan P (2006) A normative perspective on motivation. Trends Cogn Sci 10:375–381

    Article  PubMed  Google Scholar 

  • O’Doherty J, Dayan P, Schultz J, Deichmann R, Friston K, Dolan RJ (2004) Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 304:452–454

    Article  PubMed  Google Scholar 

  • O’Reilly RC (2006) Biologically based computational models of high-level cognition. Science 314:91–94

    Article  PubMed  Google Scholar 

  • Pan W-X, Schmidt R, Wickens JR, Hyland BI (2005) Dopamine cells respond to predicted events during classical conditioning: evidence for eligibility traces in the reward-learning network. J Neurosci 25:6235–6242

    Article  PubMed  CAS  Google Scholar 

  • Puterman ML (1994) Markov decision processes. Wiley, New York

    Book  Google Scholar 

  • Redgrave P, Gurney K (2006) The short-latency dopamine signal: a role in discovering novel actions? Nat Rev, Neurosci 7:967–975

    Article  CAS  Google Scholar 

  • Redgrave P, Prescott TJ, Gurney K (1999) Is the short-latency dopamine response too short to signal reward error? Trends Neurosci 22:146–151

    Article  PubMed  CAS  Google Scholar 

  • Redish AD (2004) Addiction as a computational process gone awry. Nature 306:1944–1947

    CAS  Google Scholar 

  • Redish AD, Jensen S, Johnson A (2008) A unified framework for addiction: Vulnerabilities in the decision process. Behav Brain Sci 31(4):415–437; discussion 437–487

    PubMed  Google Scholar 

  • Robinson TE, Berridge KC (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brains Res Rev 18:247–291

    Article  CAS  Google Scholar 

  • Robinson TE, Berridge KC (2003) Addiction. Annu Rev Psychol 54:25–53

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Schultz W (1998) Predictive reward signal of dopamine neurons. J Neurophysiol 80:1–27

    PubMed  CAS  Google Scholar 

  • Schultz W (2002) Getting formal with dopamine and reward. Neuron 36:241–263

    Article  PubMed  CAS  Google Scholar 

  • Schultz W, Dayan P, Montague PR (1997) A neural substrate of prediction and reward. Science 275:1593–1599

    Article  PubMed  CAS  Google Scholar 

  • Sutton RS, Barto AG (1981) Toward a modern theory of adaptive networks: expectation and prediction. Psychol Rev 88(2):135–170

    Article  PubMed  CAS  Google Scholar 

  • Tindell AJ, Berridge KC, Aldridge JW (2004) Ventral pallidal representation of pavlovian cues and reward: population and rate codes. J Neurosci 24:1058–1069

    Article  PubMed  CAS  Google Scholar 

  • Tindell AJ, Berridge KC, Zhang J, Peciña S, Aldridge JW (2005) Ventral pallidal neurons code incentive motivation: amplification by mesolimbic sensitization and amphetamine. Eur J Neurosci 22:2617–2634

    Article  PubMed  Google Scholar 

  • Tindell AJ, Smith KS, Pecina S, Berridge KC, Aldridge JW (2006) Ventral pallidum firing codes hedonic reward: when a bad taste turns good. J Neurophysiol 96(5):2399–2409

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Toates F (1986) Motivational systems. Cambridge University Press, Cambridge

    Google Scholar 

  • Zahm DS (2000) An integrative neuroanatomical perspective on some subcortical substrates of adaptive responding with emphasis on the nucleus accumbens. Neurosci Biobehav Rev 24:85–105

    Article  PubMed  CAS  Google Scholar 

  • Zahm DS (2006) The evolving theory of basal forebrain functional-anatomical ‘macrosystems’. Neurosci Biobehav Rev 30:148–172

    Article  PubMed  Google Scholar 

  • Zhang J, Berridge KC, Tindell AJ, Smith KS, Aldridge JW (2009) Modeling the neural computation of incentive salience. PLoS Comput Biol 5:1–14

    Google Scholar 

Download references

Acknowledgements

Collection of experimental data that gave rise to this computational model was supported by NIH grants DA017752, DA015188 and MH63649. The writing of this book chapter was also supported by AFOSR grant FA9550-06-1-0298. We thank Dr. Michael F.R. Robinson for helpful comments on an earlier version of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kent C. Berridge .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Zhang, J., Berridge, K.C., Aldridge, J.W. (2012). Computational Models of Incentive-Sensitization in Addiction: Dynamic Limbic Transformation of Learning into Motivation. 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_7

Download citation

Publish with us

Policies and ethics