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The alcoholic brain: neural bases of impaired reward-based decision-making in alcohol use disorders

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Abstract

Neuroeconomics is providing insights into the neural bases of decision-making in normal and pathological conditions. In the neuropsychiatric domain, this discipline investigates how abnormal functioning of neural systems associated with reward processing and cognitive control promotes different disorders, and whether such evidence may inform treatments. This endeavor is crucial when studying different types of addiction, which share a core promoting mechanism in the imbalance between impulsive subcortical neural signals associated with immediate pleasurable outcomes and inhibitory signals mediated by a prefrontal reflective system. The resulting impairment in behavioral control represents a hallmark of alcohol use disorders (AUDs), a chronic relapsing disorder characterized by excessive alcohol consumption despite devastating consequences. This review aims to summarize available magnetic resonance imaging (MRI) evidence on reward-related decision-making alterations in AUDs, and to envision possible future research directions. We review functional MRI (fMRI) studies using tasks involving monetary rewards, as well as MRI studies relating decision-making parameters to neurostructural gray- or white-matter metrics. The available data suggest that excessive alcohol exposure affects neural signaling within brain networks underlying adaptive behavioral learning via the implementation of prediction errors. Namely, weaker ventromedial prefrontal cortex activity and altered connectivity between ventral striatum and dorsolateral prefrontal cortex likely underpin a shift from goal-directed to habitual actions which, in turn, might underpin compulsive alcohol consumption and relapsing episodes despite adverse consequences. Overall, these data highlight abnormal fronto-striatal connectivity as a candidate neurobiological marker of impaired choice in AUDs. Further studies are needed, however, to unveil its implications in the multiple facets of decision-making.

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References

  1. American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders, 5th edn. American Psychiatric Publishing, Arlington, VA. https://doi.org/10.1176/appi.books.9780890425596

    Book  Google Scholar 

  2. Shield KD, Parry C, Rhem J (2013) Chronic diseases and conditions related to alcohol use. Alcohol Res 35(2):155–173

    PubMed  Google Scholar 

  3. Perry CJ (2016) Cognitive decline and recovery in alcohol abuse. J Mol Neurosci 60(3):383–389. https://doi.org/10.1007/s12031-016-0798-4

    Article  CAS  PubMed  Google Scholar 

  4. Bechara A, Damasio AR (2005) The somatic marker hypothesis: a neural theory of economic decision. Game Econ Behav 52(2):336–372. https://doi.org/10.1016/j.geb.2004.06.010

    Article  Google Scholar 

  5. Olsen VV, Lugo RG, Sutterlin S (2015) The somatic marker theory in the context of addiction: contributions to understanding development and maintenance. Psychol Res Behav Manag 8:187–200. https://doi.org/10.2147/PRBM.S68695

    PubMed  PubMed Central  Google Scholar 

  6. Liebermann MD (2007) Social cognitive neuroscience: a review of core processes. Annu Rev Psychol 58(1):259–289. https://doi.org/10.1146/annurev.psych.58.110405.085654

    Article  Google Scholar 

  7. Grueter BA, Rothwell PE, Malenka RC (2012) Integrating synaptic plasticity and striatal circuit function in addiction. Curr Opin Neurobiol 22(3):545–551. https://doi.org/10.1016/j.conb.2011.09.009

    Article  CAS  PubMed  Google Scholar 

  8. Noel X, Brevers D, Bechara A (2013) A neurocognitive approach to understanding the neurobiology of addiction. Curr Opin Neurobiol 23(4):632–638. https://doi.org/10.1016/j.conb.2013.01.018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Bechara A (2005) Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective. Nat Neurosci 8(11):1458–1463. https://doi.org/10.1038/nn1584

    Article  CAS  PubMed  Google Scholar 

  10. Koob GF (2013a) Addiction is a reward deficit and stress surfeit disorder. Front psychiatry 4:72. https://doi.org/10.3389/fpsyt.2013.00072

    Article  PubMed  PubMed Central  Google Scholar 

  11. MacKillop J (2016) The behavioral economics and neuroeconomics of alcohol use disorders. Alcohol Clin Exp Res 40(4):672–685. https://doi.org/10.1111/acer.13004

    Article  PubMed  PubMed Central  Google Scholar 

  12. Koob GF (2013b) Theoretical frameworks and mechanistic aspects of alcohol addiction: alcohol addiction as a reward deficit disorder. Curr Top Behav Neurosci 13:3–30. https://doi.org/10.1007/7854_2011_129;

    Article  PubMed  PubMed Central  Google Scholar 

  13. Sharp C, Monterosso J, Montague PR (2012) Neuroeconomics: a bridge for translational research. Biol Psychiatry 72(2):87–92. https://doi.org/10.1016/j.biopsych.2012.02.029;

    Article  PubMed  PubMed Central  Google Scholar 

  14. Chau DT, Roth RM, Green AI (2004) The neural circuitry of reward and its relevance to psychiatric disorders. Curr Psychiatry Rep 6(5):391–399. https://doi.org/10.1007/s11920-004-0026-8;

    Article  PubMed  Google Scholar 

  15. O’Doherty JP, Deichmann R, Critchley HD, Dolan RJ (2002) Neural responses during anticipation of a primary taste reward. Neuron 33(5):815–826. https://doi.org/10.1016/S0896-6273(02)00603-7;

    Article  PubMed  Google Scholar 

  16. Knutson B, Adams CM, Fong GW, Hommer D (2001) Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neurosci 21(16):RC159

    CAS  PubMed  Google Scholar 

  17. Strathearn L, Li J, Fonagy P, Montague PR (2008) What’s in a smile? Maternal brain responses to infant facial cues. Pediatrics 122(1):40–51. https://doi.org/10.1542/peds.2007-1566;

    Article  PubMed  PubMed Central  Google Scholar 

  18. Liu X, Hairston J, Schrier M, Fan J (2011) Common and distinct networks underlying reward valence and processing stages: a meta-analysis of functional neuroimaging studies. Neurosci Biobehav Rev 35(5):1219–1236. https://doi.org/10.1016/j.neubiorev.2010.12.012;

    Article  PubMed  Google Scholar 

  19. Canessa N, Crespi C, Motterlini M, Boud-Bovy G, Chierchia G, Pantaleo G, Tettamanti M, Cappa SF (2013) The functional and structural neural basis of individual differences in loss aversion. J Neurosci 33(36):14307–14317. https://doi.org/10.1523/JNEUROSCI.0497-13.2013;

    Article  CAS  PubMed  Google Scholar 

  20. 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. https://doi.org/10.1126/science.1134239

    Article  CAS  PubMed  Google Scholar 

  21. Schultz W (2015) Neuronal rewards and signals: from theories to data. Physiol Rev 95(3):853–951. https://doi.org/10.1152/physrev.00023.2014;

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Tobler PN, Christopoulos GI, O'Doherty JP, Dolan RJ, Shultz W (2009) Risk-dependent reward value signal in human prefrontal cortex. PNAS 106(17):7185–7190. https://doi.org/10.1073/pnas.0809599106;

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Canessa N, Crespi C, Baud-Bovy G, Dodich A, Falini A, Antonellis G, Cappa SF (2017) Neural markers of loss aversion in resting-state brain activity. NeuroImage 1(146):257–265. https://doi.org/10.1016/j.neuroimage.2016.11.050;

    Article  Google Scholar 

  24. Kahneman D, Tversky A (1979) Prospect theory: an analysis of decision under risk. Econometrica 47(2):263–292. https://doi.org/10.2307/1914185

    Article  Google Scholar 

  25. Bjork JM, Momenan R, Smith AR, Hommer DW (2008b) Reduced posterior mesofrontal cortex activation by risky rewards in substance-dependent patients. Drug Alcohol Depend 95(1–2):115–128. https://doi.org/10.1016/j.drugalcdep.2007.12.014

    Article  PubMed  PubMed Central  Google Scholar 

  26. Park SQ, Kahnt T, Beck A, Choen MX, Dolan RJ, Wrase J, Heinz A (2010) Prefrontal cortex fails to learn reward prediction errors in alcohol dependence. J Neurosci 30(22):7749–7753. https://doi.org/10.1523/JNEUROSCI.5587-09.2010;

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. von Neumann J, Morgenstern O (1944) Theory of games and economic behavior. Princeton, Princeton Univ. Press

    Google Scholar 

  28. Sutton, RS.; Barto, AG. Reinforcement learning: an introduction. Cambridge: MIT Press; 1998;

  29. Knutson B, Huttel S (2016) The risk matrix. Curr Opin Behav Sci 5:141–146. https://doi.org/10.1016/j.cobeha.2015.10.012

    Article  Google Scholar 

  30. Levy DJ, Glimcher PW (2012) The root of all value: a neural common currency for choice. Curr Op Neuobiol 22(6):1027–1038. https://doi.org/10.1016/j.conb.2012.06.001

    Article  CAS  Google Scholar 

  31. Basten U, Biele G, Heekeren HR, Fiebach CJ (2010) How the brain integrates costs and benefits decision making. PNAS 107(50):21767–21772. https://doi.org/10.1073/pnas.0908104107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Warse J, Schlagenhauf F, Kienast T, Wustenberg T, Bermpohl F, Kahnt T, Beck A, Strohle A, Juckel G, Knutson B, Heinz A (2007) Dysfunction of reward processing correlates with alcohol craving in detoxified alcoholics. NeuroImage 35:787–794. https://doi.org/10.1016/j.neuroimage.2006.11.043;

    Article  Google Scholar 

  33. Beck A, Schlagenhauf F, Wustenberg T, Hein J, Kienast T, Kahnt T, Schmack K, Hagele C, Knutson B, Heinz A, Wrase J (2009) Ventral striatal activation during reward anticipation correlates with impulsivity in alcoholics. Biol Psychiatry 66(8):734–742. https://doi.org/10.1016/j.biopsych.2009.04.035;

    Article  CAS  PubMed  Google Scholar 

  34. Hagele C, Schlagenhauf F, Rapp M, Sterzer P, Beck A, Bermpohl F, Stoy M, Strohle A, Wittchen HU, Dolan RJ, Heinz A (2015) Dimensional psychiatry: reward dysfunction and depressive mood across psychiatry disorders. Psychopharmacology 232(2):331–341. https://doi.org/10.1007/s00213-014-3662-7;

    Article  PubMed  Google Scholar 

  35. Romanczuk-Seiferth N, Koehler S, Dreesen C, Wustenberg T, Heinz A (2015) Pathological gambling and alcohol dependence: neural disturbances in reward and loss avoidance processing. Addict Biol 20(3):557–569. https://doi.org/10.1111/adb.12144;

    Article  PubMed  Google Scholar 

  36. Grodin EN, Steckler LE, Momenan R (2016) Altered striatal response during effort-based valuation and motivation in alcohol-dependent individuals. Alcohol Alcoholism 51(6):638–646. https://doi.org/10.1093/alcalc/agw003

    Article  PubMed  PubMed Central  Google Scholar 

  37. Bjork JM, Smith AR, Hommer DW (2008a) Striatal sensitivity to reward deliveries and omission in substance dependent patients. NeuroImage 42(4):1609–1621. https://doi.org/10.1016/j.neuroimage.2008.06.035

    Article  PubMed  PubMed Central  Google Scholar 

  38. Bjork JM, Smith AR, Chen G, Hommer DW (2012) Mesolimbic recruitment by nondrug rewards in detoxified alcoholics: effort anticipation, reward anticipation and reward delivery. Hum Brain Mapp 33(9):2174–2188. https://doi.org/10.1002/hbm.21351;

    Article  PubMed  PubMed Central  Google Scholar 

  39. van Holst RJ, Clark L, Veltman DJ, van den Brink W, Gourdriaan AE (2014) Enached striatal responses during expetancy coding in alcohol dependence. Drug Alcohol Depend 142:204–208. https://doi.org/10.1016/j.drugalcdep.2014.06.019;

    Article  PubMed  Google Scholar 

  40. Gilman JM, Smith AR, Bjork JM, Ramchanadi VA, Momenan R, Hommer DW (2014) Cumulative gains enhance striatal response to reward opportunities in alcohol-dependent patients. Addict Biol 20(3):580–593. https://doi.org/10.1111/adb.12147

    Article  PubMed  PubMed Central  Google Scholar 

  41. Zhu X, Sundby K, Bjork JM, Momenan R (2016) Alcohol dependence and altered engagement of brain networks in risky decisions. Front Hum Neurosci 10:142. https://doi.org/10.3389/fnhum.2016.00142

    PubMed  PubMed Central  Google Scholar 

  42. Rolls ET (2013) Emotion and decision making explained. Oxford University Press, Oxford. https://doi.org/10.1093/acprof:oso/9780199659890.001.0001

    Book  Google Scholar 

  43. McClure S, Daw ND, Montague PR (2003) A computational substrate for incentive salience. Trends Neurosci 26(8):423–428. https://doi.org/10.1016/S0166-2236(03)00177-2

    Article  CAS  PubMed  Google Scholar 

  44. Pessiglione M, Seymour B, Flandin G, Dolan R, Frith CD (2006) Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans. Nature 442(7106):1042–1045. https://doi.org/10.1038/nature05051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. O’Doherty J, Critchlet H, Deichmann R, Dolan RJ (2003) Dissociating valence of outcome from behavioral control in human orbital and ventral prefrontal cortices. J Neurosci 23(21):7931–7939

    PubMed  Google Scholar 

  46. Palminteri S, Khamassi M, Joffily M, Coricelli G (2015) Contextual modulation of value signals in reward and punishment learning. Nat Commun 6:8096. https://doi.org/10.1038/ncomms9096;

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Christaku A, Brammer M, Giampietro V, Rubia K (2009) Right ventromedial and dorsolateral prefrontal cortices mediate adaptive decisions under ambiguity by integrating choice utility and outcome evaluation. J Neurosci 29(35):11020–11028. https://doi.org/10.1523/JNEUROSCI.1279-09.2009;

    Article  Google Scholar 

  48. Daw ND, O'Doherty JP, Dayan P, Seymour B, Dolan RJ (2006) Cortical substrates for exploratory decisions in humans. Nature 441(7095):876–879. https://doi.org/10.1038/nature04766;

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Laureiro-Martínez D, Canessa N, Brusoni S, Zollo M, Hare T, Alemanno F, Cappa SF (2014) Frontopolar cortex and decision-making efficiency: comparing brain activity of experts with different professional background during an exploration-exploitation task. Front Hum Neurosci 7:927. https://doi.org/10.3389/fnhum.2013.00927

    Article  PubMed  PubMed Central  Google Scholar 

  50. Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ (1997) Psycho-physiological and modulatory interactions in neuroimaging. NeuroImage 6(3):218–229. https://doi.org/10.1006/nimg.1997.0291;

    Article  CAS  PubMed  Google Scholar 

  51. Forbes EE, Rodriguez EE, Musselman NR (2014) Prefrontal response and frontostriatal functional connectivity to monetary reward in abstinent alcohol-dependent young adults. PLoS One 9(5):e94640. https://doi.org/10.1371/journal.pone.0094640

    Article  PubMed  PubMed Central  Google Scholar 

  52. Deserno L, Beck A, Huys QJM et al (2014) Chronic alcohol intake abolishes the relationship between dopamine synthesis capacity and learning signals in ventral striatum. Eur J Neurosci 41(4):477–486. https://doi.org/10.1111/ejn.12802;

    Article  PubMed  PubMed Central  Google Scholar 

  53. Reiter AMF, Deserno L, Kallert T, Heinz HJ, Heinz A, Schlagenhauf F (2016) Behavioral and neural signatures of reduced updating of alternative options in alcohol-dependent patients during flexible decision-making. J Neurosci 36(43):10935–10948. https://doi.org/10.1523/JNEUROSCI.4322-15.2016

    Article  CAS  PubMed  Google Scholar 

  54. Balta S, Beck A, Deserno L, Lorenz RC, Rapp MA, Schlagenhauf F, Heinz A, Obermayer K (2017) Dorsolateral prefrontal cortex contributes to the impaired behavioral adaptation in alcohol dependence. NeuroImage Clin 15:80–94. https://doi.org/10.1016/j.nicl.2017.04.010

    Article  Google Scholar 

  55. Sebold M, Nebe S, Garbusow M et al (2017) When habits are dangerous: alcohol expectancies and habitual decision making predict relapse in alcohol dependence. Biol Psychiatry 25:1–10. https://doi.org/10.1016/j.biopsych.2017.04.019;

    Google Scholar 

  56. Lohrenz T, McCabe K, Camerer CF, Montague PR (2007) Neural signature of fictive learning signals in a sequential investment task. Proc Natl Acad Sci 104(22):9493–9498. https://doi.org/10.1073/pnas.0608842104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Camille N, Coricelli G, Sallet J, Pradat-Diehl P, Duhamel JR, Sirigu A (2004) The involvement of the orbitofrontal cortex in the experience of regret. Science 304(5674):1167–1170. https://doi.org/10.1126/science.1094550

    Article  CAS  PubMed  Google Scholar 

  58. Canessa N, Motterlini M, Di Dio C, Perani D, Scifo P, Cappa SF, Rizzolati G (2009) Understanding others’ regret: a FMRI study. PLoS One 4(10):e7402. https://doi.org/10.1371/journal.pone.0007402;

    Article  PubMed  PubMed Central  Google Scholar 

  59. Canessa N, Motterlini M, Alemanno F, Perani D, Cappa SF (2011) Learning from other people’s experience: a neuroimaging study of decisional interactive-learning. NeuroImage 55(1):353–362. https://doi.org/10.1016/j.neuroimage.2010.11.065;

    Article  PubMed  Google Scholar 

  60. Gläscher J, Daw N, 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. https://doi.org/10.1016/j.neuron.2010.04.016

    Article  PubMed  PubMed Central  Google Scholar 

  61. Daw ND, Gershman SJ, Seymour B, Dayan P, Dolan RJ Model-based influences on humans’ choices and striatal prediction errors. Neuron 69(6):1204–1215. https://doi.org/10.1016/j.neuron.2011.02.027

  62. Valentin VV, Dickinson A, O'Doherty JP (2007) Determining the neural substrates of goal-directed learning in the human brain. J Neurosci 27(15):4019–4026. https://doi.org/10.1523/JNEUROSCI.0564-07.2007;

    Article  CAS  PubMed  Google Scholar 

  63. Tricomi E, Balleine BW, O'Doherty JP (2009) A specific role for posterior dorsolateral striatum in human habit learning. Eur J Neurosci 29(11):2225–2232. https://doi.org/10.1111/j.1460-9568.2009.06796.x;

    Article  PubMed  PubMed Central  Google Scholar 

  64. de Wit S, Watson P, Harsay HA, Cohen MX, van de Vijver I, Ridderinkhof KR (2012) Corti-costriatal connectivity underlies individual differences in the balance between habitual and goal-directed action control. J Neurosci 32(35):12066–12075. https://doi.org/10.1523/JNEUROSCI.1088-12.2012

    Article  PubMed  Google Scholar 

  65. Newline DB, Strubler KA (2007) The habitual brain: an “adapted habit” theory of substance use disorders. Subst Use Misuse 42(2–3):503–526. https://doi.org/10.1080/10826080601144606

    Article  Google Scholar 

  66. Sjoerds Z, de Wit S, van den Brink W, Robbinson TW, Beekman ATF, Penninx BWJH, Veltman DJ (2013) Behavioral and neuroimaging evidence for overreliance on habit learning in alcohol-dependent patients. Transl Psychiatry 3(12):e337. https://doi.org/10.1038/tp.2013.107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Lee D, Seo H, Jung MW (2012) Neural basis of reinforcement learning and decision making. Annu Rev Neurosci 35(1):287–308. https://doi.org/10.1146/annurev-neuro-062111-150512;

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Ames SL, Grenard JL, He Q, Stacy AW, Wong SW, Xiao L, Xue G, Bechara A (2014) Functional imaging of an alcohol-implicit association test (IAT). Addict Biol 19(3):467–481. https://doi.org/10.1111/adb.12071;

    Article  PubMed  Google Scholar 

  69. Greenwald AG, McGhee DE, Schwartz JLK (1998) Measuring individual differences in implicit cognition: the implicit association test. J Pers Soc Psychol 74(6):1464–1480. https://doi.org/10.1037/0022-3514.74.6.1464;

    Article  CAS  PubMed  Google Scholar 

  70. Makris N, Oscar-Berman M, Jaffin SK, Hodge SM, Kennedy DN, Caviness VS, Marinkovic K, Breiter HC, Gasic GP, Harris GJ (2008) Decreased volume of the brain reward system in alcoholism. Biol Psychiatry 64(3):192–202. https://doi.org/10.1016/j.biopsych.2008.01.018;

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Le Berre AP, Rauchs G, La Joie R, Mezenge F, Boudehent C et al (2014) Impaired decision-making and brain shrinkage in alcoholism. Eur Psychiatry 29(3):125–133. https://doi.org/10.1016/j.eurpsy.2012.10.002

    Article  PubMed  Google Scholar 

  72. Fein G, Landman B, Tran H, McGillivrat S, Finn P, Barakos J, Moon K (2006) Brain atrophy in long-term abstinent alcoholics who demonstrate impairment on a simulated gambling task. NeuroImage 32(3):1465–1471. https://doi.org/10.1016/j.neuroimage.2006.06.013;

    Article  PubMed  PubMed Central  Google Scholar 

  73. Bechara A, Damasio AR, Damasio H, Anderson SW (1994) Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50(1-3):7–15. https://doi.org/10.1016/0010-0277(94)90018-3;

    Article  CAS  PubMed  Google Scholar 

  74. Zorlu N, Gelal F, Kuserli A, Cenik E, Durmaz E, Saricicek A, Gulseren S (2013) Abnormal white matter integrity and decision-making deficits in alcohol dependence. Psychiatry Res 214(3):382–388. https://doi.org/10.1016/j.pscychresns.2013.06.014;

    Article  PubMed  Google Scholar 

  75. Zorlu N, Ucman TK, Gelal F, Kalayci CC, Polat S, Saricicek A, Zorlu PK, Gulseren S (2014) Abnormal white matte integrity in long-term abstinent alcohol dependent patients. Psychiatry Res 224(1):42–48. https://doi.org/10.1016/j.pscychresns.2014.07.006

    Article  PubMed  Google Scholar 

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Galandra, C., Basso, G., Cappa, S. et al. The alcoholic brain: neural bases of impaired reward-based decision-making in alcohol use disorders. Neurol Sci 39, 423–435 (2018). https://doi.org/10.1007/s10072-017-3205-1

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