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Translational Research on Habit and Alcohol

  • Alcohol (RF Leeman, Section Editor)
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Abstract

Habitual actions enable efficient daily living, but they can also contribute to pathological behaviors that are resistant to change, such as alcoholism. Habitual behaviors are learned actions that appear goal-directed but are in fact no longer under the control of the action’s outcome. Instead, these actions are triggered by stimuli, which may be exogenous or interoceptive, discrete or contextual. A major hallmark characteristic of alcoholism is continued alcohol use despite serious negative consequences. In essence, although the outcome of alcohol seeking and drinking is dramatically devalued, these actions persist, often triggered by environmental cues associated with alcohol use. Thus, alcoholism meets the definition of an initially goal-directed behavior that converts to a habit-based process. Habit and alcohol have been well investigated in rodent models, with comparatively less research in non-human primates and people. This review focuses on translational research on habit and alcohol with an emphasis on cross-species methodology and neural circuitry.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. Dickinson A. Actions and habits- the development of behavioral autonomy. Philos Trans R Soc Lond Ser B Biol Sci. 1985;308(1135):67–78.

    Article  Google Scholar 

  2. Kalivas PW. Addiction as a pathology in prefrontal cortical regulation of corticostriatal habit circuitry. Neurotox Res. 2008;14(2-3):185–9.

    Article  PubMed  Google Scholar 

  3. Kehagia AA, Murray GK, Robbins TW. Learning and cognitive flexibility: frontostriatal function and monoaminergic modulation. Curr Opin Neurobiol. 2010;20(2):199–204.

    Article  PubMed  CAS  Google Scholar 

  4. de Wit S et al. Stimulus-outcome interactions during instrumental discrimination learning by rats and humans. J Exp Psychol Anim Behav Process. 2007;33(1):1–11.

    Article  PubMed  Google Scholar 

  5. Hadj-Bouziane F et al. Advanced Parkinson’s disease effect on goal-directed and habitual processes involved in visuomotor associative learning. Front Hum Neurosci. 2012;6:351.

    PubMed Central  PubMed  Google Scholar 

  6. Noonan MP, Mars RB, Rushworth MF. Distinct roles of three frontal cortical areas in reward-guided behavior. J Neurosci. 2011;31(40):14399–412.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  7. Petrides M. Motor conditional associative-learning after selective prefrontal lesions in the monkey. Behav Brain Res. 1982;5(4):407–13.

    Article  PubMed  CAS  Google Scholar 

  8. Petrides M. Deficits on conditional associative-learning tasks after frontal- and temporal-lobe lesions in man. Neuropsychologia. 1985;23(5):601–14.

    Article  PubMed  CAS  Google Scholar 

  9. Petrides M. Visuo-motor conditional associative learning after frontal and temporal lesions in the human brain. Neuropsychologia. 1997;35(7):989–97.

    Article  PubMed  CAS  Google Scholar 

  10. Murray EA, Bussey TJ, Wise SP. Role of prefrontal cortex in a network for arbitrary visuomotor mapping. Exp Brain Res. 2000;133(1):114–29.

    Article  PubMed  CAS  Google Scholar 

  11. Naneix F et al. A role for medial prefrontal dopaminergic innervation in instrumental conditioning. J Neurosci. 2009;29(20):6599–606.

    Article  PubMed  CAS  Google Scholar 

  12. Stalnaker TA et al. Neural correlates of stimulus-response and response-outcome associations in dorsolateral versus dorsomedial striatum. Front Integr Neurosci. 2010;4:12.

    Article  PubMed Central  PubMed  Google Scholar 

  13. Farovik A et al. Medial prefrontal cortex supports recollection, but not familiarity, in the rat. J Neurosci. 2008;28(50):13428–34.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  14. Coutureau E, Killcross S. Inactivation of the infralimbic prefrontal cortex reinstates goal-directed responding in overtrained rats. Behav Brain Res. 2003;146(1-2):167–74.

    Article  PubMed  Google Scholar 

  15. Izquierdo A, Jentsch JD. Reversal learning as a measure of impulsive and compulsive behavior in addictions. Psychopharmacology (Berlin). 2012;219(2):607–20.

    Article  CAS  Google Scholar 

  16. Killcross S, Coutureau E. Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb Cortex. 2003;13(4):400–8.

    Article  PubMed  Google Scholar 

  17. Rhodes SE, Murray EA. Differential effects of amygdala, orbital prefrontal cortex, and prelimbic cortex lesions on goal-directed behavior in rhesus macaques. J Neurosci. 2013;33(8):3380–9.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  18. Smith KS et al. Reversible online control of habitual behavior by optogenetic perturbation of medial prefrontal cortex. Proc Natl Acad Sci U S A. 2012;109(46):18932–7.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  19. Tran-Tu-Yen DA et al. Transient role of the rat prelimbic cortex in goal-directed behaviour. Eur J Neurosci. 2009;30(3):464–71.

    Article  PubMed  Google Scholar 

  20. Yin HH, Knowlton BJ, Balleine BW. Inactivation of dorsolateral striatum enhances sensitivity to changes in the action-outcome contingency in instrumental conditioning. Behav Brain Res. 2006;166(2):189–96.

    Article  PubMed  Google Scholar 

  21. Yin HH, Ostlund SB, Balleine BW. Reward-guided learning beyond dopamine in the nucleus accumbens: the integrative functions of cortico-basal ganglia networks. Eur J Neurosci. 2008;28(8):1437–48.

    Article  PubMed Central  PubMed  Google Scholar 

  22. Yin HH et al. The role of the dorsomedial striatum in instrumental conditioning. Eur J Neurosci. 2005;22(2):513–23.

    Article  PubMed  Google Scholar 

  23. Yin HH, Knowlton BJ, Balleine BW. Blockade of NMDA receptors in the dorsomedial striatum prevents action-outcome learning in instrumental conditioning. Eur J Neurosci. 2005;22(2):505–12.

    Article  PubMed  Google Scholar 

  24. Asaad WF, Rainer G, Miller EK. Neural activity in the primate prefrontal cortex during associative learning. Neuron. 1998;21(6):1399–407.

    Article  PubMed  CAS  Google Scholar 

  25. Asaad WF, Rainer G, Miller EK. Task-specific neural activity in the primate prefrontal cortex. J Neurophysiol. 2000;84(1):451–9.

    PubMed  CAS  Google Scholar 

  26. Fusi S et al. A neural circuit model of flexible sensorimotor mapping: learning and forgetting on multiple timescales. Neuron. 2007;54(2):319–33.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  27. Toni I et al. Learning arbitrary visuomotor associations: temporal dynamic of brain activity. Neuroimage. 2001;14(5):1048–57.

    Article  PubMed  CAS  Google Scholar 

  28. Muhammad R, Wallis JD, Miller EK. A comparison of abstract rules in the prefrontal cortex, premotor cortex, inferior temporal cortex, and striatum. J Cogn Neurosci. 2006;18(6):974–89.

    Article  PubMed  Google Scholar 

  29. Wallis JD, Anderson KC, Miller EK. Single neurons in prefrontal cortex encode abstract rules. Nature. 2001;411(6840):953–6.

    Article  PubMed  CAS  Google Scholar 

  30. Wallis JD, Miller EK. From rule to response: neuronal processes in the premotor and prefrontal cortex. J Neurophysiol. 2003;90(3):1790–806.

    Article  PubMed  Google Scholar 

  31. Loh M et al. Neurodynamics of the prefrontal cortex during conditional visuomotor associations. J Cogn Neurosci. 2008;20(3):421–31.

    Article  PubMed  Google Scholar 

  32. Pasupathy A, Miller EK. Different time courses of learning-related activity in the prefrontal cortex and striatum. Nature. 2005;433(7028):873–6.

    Article  PubMed  CAS  Google Scholar 

  33. Boettiger CA, D’Esposito M. Frontal networks for learning and executing arbitrary stimulus-response associations. J Neurosci. 2005;25(10):2723–32.

    Article  PubMed  CAS  Google Scholar 

  34. de Wit S et al. Differential engagement of the ventromedial prefrontal cortex by goal-directed and habitual behavior toward food pictures in humans. J Neurosci. 2009;29(36):11330–8.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  35. Valentin VV, Dickinson A, O’Doherty JP. Determining the neural substrates of goal-directed learning in the human brain. J Neurosci. 2007;27(15):4019–26.

    Article  PubMed  CAS  Google Scholar 

  36. Tricomi E, Balleine BW, O’Doherty JP. A specific role for posterior dorsolateral striatum in human habit learning. Eur J Neurosci. 2009;29(11):2225–32.

    Article  PubMed Central  PubMed  Google Scholar 

  37. Association AP. Diagnostic and statistical manual of mental disorders. 4th ed., text rev. ed. Washington, DC; 2000.

  38. Ostlund SB, Balleine BW. On habits and addiction: an associative analysis of compulsive drug seeking. Drug Discov Today Dis Models. 2008;5(4):235–45.

    Article  PubMed Central  PubMed  Google Scholar 

  39. Belin D et al. Addiction: failure of control over maladaptive incentive habits. Curr Opin Neurobiol. 2013;23(4):564–72.

    Article  PubMed  CAS  Google Scholar 

  40. Balleine BW, O’Doherty JP. Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology. 2010;35(1):48–69.

    Article  PubMed Central  PubMed  Google Scholar 

  41. Adams CD, Dickinson A. Instrumental responding following reinforcer devaluation. Q J Exp Psychol B Comp Physiol Psychol. 1981;33:109–21.

    Article  Google Scholar 

  42. Koob GF, Volkow ND. Neurocircuitry of addiction. Neuropsychopharmacology. 2010;35(1):217–38.

    Article  PubMed Central  PubMed  Google Scholar 

  43. Belin-Rauscent A, Everitt BJ, Belin D. Intrastriatal shifts mediate the transition from drug-seeking actions to habits. Biol Psychiatry. 2012;72(5):343–5.

    Article  PubMed  Google Scholar 

  44. Hogarth L et al. Associative learning mechanisms underpinning the transition from recreational drug use to addiction. Ann N Y Acad Sci. 2013;1282(1):12–24.

    Article  PubMed  CAS  Google Scholar 

  45. Desrochers TM, Amemori K, Graybiel AM. Habit learning by naive macaques is marked by response sharpening of striatal neurons representing the cost and outcome of acquired action sequences. Neuron. 2015;87(4):853–68.

    Article  PubMed  CAS  Google Scholar 

  46. Izquierdo A, Suda RK, Murray EA. Bilateral orbital prefrontal cortex lesions in rhesus monkeys disrupt choices guided by both reward value and reward contingency. J Neurosci. 2004;24(34):7540–8.

    Article  PubMed  CAS  Google Scholar 

  47. Fernandez-Ruiz J et al. Visual habit formation in monkeys with neurotoxic lesions of the ventrocaudal neostriatum. Proc Natl Acad Sci U S A. 2001;98(7):4196–201.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  48. Miyachi S, Hikosaka O, Lu X. Differential activation of monkey striatal neurons in the early and late stages of procedural learning. Exp Brain Res. 2002;146(1):122–6.

    Article  PubMed  Google Scholar 

  49. Deffains M, Legallet E, Apicella P. Modulation of neuronal activity in the monkey putamen associated with changes in the habitual order of sequential movements. J Neurophysiol. 2010;104(3):1355–69.

    Article  PubMed  Google Scholar 

  50. Hikosaka O et al. Learning of sequential movements in the monkey: process of learning and retention of memory. J Neurophysiol. 1995;74(4):1652–61.

    PubMed  CAS  Google Scholar 

  51. Kim HF, Hikosaka O. Parallel basal ganglia circuits for voluntary and automatic behaviour to reach rewards. Brain. 2015;138(Pt 7):1776–800.

    Article  PubMed  Google Scholar 

  52. Hikosaka O et al. Central mechanisms of motor skill learning. Curr Opin Neurobiol. 2002;12(2):217–22.

    Article  PubMed  CAS  Google Scholar 

  53. Fanelli RR et al. Dorsomedial and dorsolateral striatum exhibit distinct phasic neuronal activity during alcohol self-administration in rats. Eur J Neurosci. 2013;38(4):2637–48.

    Article  PubMed Central  PubMed  Google Scholar 

  54. Gremel CM, Costa RM. Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual actions. Nat Commun. 2013;4:2264.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  55. Hay RA et al. Specific and nonspecific effects of naltrexone on goal-directed and habitual models of alcohol seeking and drinking. Alcohol Clin Exp Res. 2013;37(7):1100–10.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  56. Mangieri RA, Cofresi RU, Gonzales RA. Ethanol seeking by Long Evans rats is not always a goal-directed behavior. PLoS One. 2012;7(8):e42886.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  57. Corbit LH, Nie H, Janak PH. Habitual alcohol seeking: time course and the contribution of subregions of the dorsal striatum. Biol Psychiatry. 2012;72(5):389–95. A thorough study demonstrating that chronic alcohol drinking can promote habitual alcohol- and sucrose-seeking behavior in a rodent operant model.

    Article  PubMed Central  PubMed  Google Scholar 

  58. Everitt BJ, Robbins TW. Second-order schedules of drug reinforcement in rats and monkeys: measurement of reinforcing efficacy and drug-seeking behaviour. Psychopharmacology (Berlin). 2000;153(1):17–30.

    Article  CAS  Google Scholar 

  59. Negus SS, Mello NK. Effects of chronic d-amphetamine treatment on cocaine- and food-maintained responding under a second-order schedule in rhesus monkeys. Drug Alcohol Depend. 2003;70(1):39–52.

    Article  PubMed  CAS  Google Scholar 

  60. Lamb RJ, Pinkston JW, Ginsburg BC. Ethanol self-administration in mice under a second-order schedule. Alcohol. 2015;49(6):561–70.

    Article  PubMed  CAS  Google Scholar 

  61. Belin D, Everitt BJ. Cocaine seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum. Neuron. 2008;57(3):432–41.

    Article  PubMed  CAS  Google Scholar 

  62. Kaminski BJ et al. Dissociation of alcohol-seeking and consumption under a chained schedule of oral alcohol reinforcement in baboons. Alcohol Clin Exp Res. 2008;32(6):1014–22.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  63. Olmstead MC et al. Cocaine seeking by rats is a goal-directed action. Behav Neurosci. 2001;115(2):394–402.

    Article  PubMed  CAS  Google Scholar 

  64. Zapata A, Minney VL, Shippenberg TS. Shift from goal-directed to habitual cocaine seeking after prolonged experience in rats. J Neurosci. 2010;30(46):15457–63.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  65. Balleine BW, Dickinson A. Goal-directed instrumental action: contingency and incentive learning and their cortical substrates. Neuropharmacology. 1998;37(4-5):407–19.

    Article  PubMed  CAS  Google Scholar 

  66. Shillinglaw JE, Everitt IK, Robinson DL. Assessing behavioral control across reinforcer solutions on a fixed-ratio schedule of reinforcement in rats. Alcohol. 2014;48(4):337–44.

    Article  PubMed Central  PubMed  Google Scholar 

  67. Wellman LL, Gale K, Malkova L. GABAA-mediated inhibition of basolateral amygdala blocks reward devaluation in macaques. J Neurosci. 2005;25(18):4577–86.

    Article  PubMed  Google Scholar 

  68. Soares JM et al. Stress-induced changes in human decision-making are reversible. Transl Psychiatry. 2012;2:e131.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  69. de Wit S et al. Corticostriatal connectivity underlies individual differences in the balance between habitual and goal-directed action control. J Neurosci. 2012;32(35):12066–75.

    Article  PubMed  CAS  Google Scholar 

  70. Gillan CM et al. Disruption in the balance between goal-directed behavior and habit learning in obsessive-compulsive disorder. Am J Psychiatr. 2011;168(7):718–26.

    Article  PubMed Central  PubMed  Google Scholar 

  71. Deiber MP et al. Frontal and parietal networks for conditional motor learning: a positron emission tomography study. J Neurophysiol. 1997;78(2):977–91.

    PubMed  CAS  Google Scholar 

  72. Dolan RJ, Dayan P. Goals and habits in the brain. Neuron. 2013;80(2):312–25. Recent review of goal-directed and habitual behavior, with emphasis on computational modeling.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  73. Friedel E et al. Devaluation and sequential decisions: linking goal-directed and model-based behavior. Front Hum Neurosci. 2014;8:9. The authors tested the correspondence between the current task designs used to assess goal-directed and habitual behavior in the lab, finding similarities in model-based and goal-directed behavior.

    Article  Google Scholar 

  74. Daw ND et al. Model-based influences on humans’ choices and striatal prediction errors. Neuron. 2011;69(6):1204–15.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  75. Smith KS, Graybiel AM. Investigating habits: strategies, technologies and models. Front Behav Neurosci. 2014;8:39.

    PubMed Central  PubMed  Google Scholar 

  76. Ashby FG, Turner BO, Horvitz JC. Cortical and basal ganglia contributions to habit learning and automaticity. Trends Cogn Sci. 2010;14(5):208–15.

    Article  PubMed Central  PubMed  Google Scholar 

  77. 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(1):181–9.

    Article  PubMed  Google Scholar 

  78. Smith KS, Graybiel AM. A dual operator view of habitual behavior reflecting cortical and striatal dynamics. Neuron. 2013;79(2):361–74. This study used real-time electrophysiology to simultaneously monitor neurons in the dorsolateral striatum and the infralimbic cortex of rats during the transition from a goal-directed to a habitual behavior.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  79. Voorn P et al. Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci. 2004;27(8):468–74.

    Article  PubMed  CAS  Google Scholar 

  80. Keistler C, Barker JM, Taylor JR. Infralimbic prefrontal cortex interacts with nucleus accumbens shell to unmask expression of outcome-selective Pavlovian-to-instrumental transfer. Learn Mem. 2015;22(10):509–13.

    Article  PubMed  Google Scholar 

  81. Baxter MG et al. Control of response selection by reinforcer value requires interaction of amygdala and orbital prefrontal cortex. J Neurosci. 2000;20(11):4311–9.

    PubMed  CAS  Google Scholar 

  82. Nauta WJ. Fibre degeneration following lesions of the amygdaloid complex in the monkey. J Anat. 1961;95:515–31.

    PubMed Central  PubMed  CAS  Google Scholar 

  83. Aggleton JP, et al. Complementary patterns of direct amygdala and hippocampal projections to the macaque prefrontal cortex. Cerebral Cortex. 2015; p. bhv019.

  84. Porrino LJ, Crane AM, Goldman-Rakic PS. Direct and indirect pathways from the amygdala to the frontal lobe in rhesus monkeys. J Comp Neurol. 1981;198(1):121–36.

    Article  PubMed  CAS  Google Scholar 

  85. Balleine BW, Killcross AS, Dickinson A. The effect of lesions of the basolateral amygdala on instrumental conditioning. J Neurosci. 2003;23(2):666–75.

    PubMed  CAS  Google Scholar 

  86. Lingawi NW, Balleine BW. Amygdala central nucleus interacts with dorsolateral striatum to regulate the acquisition of habits. J Neurosci. 2012;32(3):1073–81.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  87. Kelley AE, Domesick VB, Nauta WJ. The amygdalostriatal projection in the rat–an anatomical study by anterograde and retrograde tracing methods. Neuroscience. 1982;7(3):615–30.

    Article  PubMed  CAS  Google Scholar 

  88. Rouillard C, Freeman AS. Effects of electrical stimulation of the central nucleus of the amygdala on the in vivo electrophysiological activity of rat nigral dopaminergic neurons. Synapse. 1995;21(4):348–56.

    Article  PubMed  CAS  Google Scholar 

  89. O’Doherty JP. Contributions of the ventromedial prefrontal cortex to goal-directed action selection. Ann N Y Acad Sci. 2011;1239:118–29.

    Article  PubMed  Google Scholar 

  90. Mattfeld AT, Gluck MA, Stark CE. Functional specialization within the striatum along both the dorsal/ventral and anterior/posterior axes during associative learning via reward and punishment. Learn Mem. 2011;18(11):703–11.

    Article  PubMed Central  PubMed  Google Scholar 

  91. Tanaka SC, Balleine BW, O’Doherty JP. Calculating consequences: brain systems that encode the causal effects of actions. J Neurosci. 2008;28(26):6750–5.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  92. Tricomi EM, Delgado MR, Fiez JA. Modulation of caudate activity by action contingency. Neuron. 2004;41(2):281–92.

    Article  PubMed  CAS  Google Scholar 

  93. Sjoerds Z et al. Behavioral and neuroimaging evidence for overreliance on habit learning in alcohol-dependent patients. Transl Psychiatry. 2013;3:e337.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  94. Lee SW, Shimojo S, O’Doherty JP. Neural computations underlying arbitration between model-based and model-free learning. Neuron. 2014;81(3):687–99.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  95. Smittenaar P et al. Disruption of dorsolateral prefrontal cortex decreases model-based in favor of model-free control in humans. Neuron. 2013;80(4):914–9. Direct manipulation of prefrontal brain function via TMS demonstrating the importance of cortical regulation on striatally driven habitual action selection.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  96. Smittenaar P et al. Transcranial direct current stimulation of right dorsolateral prefrontal cortex does not affect model-based or model-free reinforcement learning in humans. Plos One. 2014;9(1):8.

    Article  CAS  Google Scholar 

  97. de Wit S et al. Reliance on habits at the expense of goal-directed control following dopamine precursor depletion. Psychopharmacology. 2012;219(2):621–31.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  98. Wunderlich K, Smittenaar P, Dolan RJ. Dopamine enhances model-based over model-free choice behavior. Neuron. 2012;75(3):418–24.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  99. Crews FT et al. Effects of ethanol on ion channels. Int Rev Neurobiol. 1996;39:283–367.

    Article  PubMed  CAS  Google Scholar 

  100. Woodward JJ. Ethanol and NMDA receptor signaling. Crit Rev Neurobiol. 2000;14(1):69–89.

    Article  PubMed  CAS  Google Scholar 

  101. Lovinger DM, Partridge JG, Tang KC. Plastic control of striatal glutamatergic transmission by ensemble actions of several neurotransmitters and targets for drugs of abuse. Ann N Y Acad Sci. 2003;1003:226–40.

    Article  PubMed  CAS  Google Scholar 

  102. Vengeliene V et al. Neuropharmacology of alcohol addiction. Br J Pharmacol. 2008;154(2):299–315.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  103. Chen G et al. Striatal involvement in human alcoholism and alcohol consumption, and withdrawal in animal models. Alcohol Clin Exp Res. 2011;35(10):1739–48.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  104. Lovinger DM, White G, Weight FF. NMDA receptor-mediated synaptic excitation selectively inhibited by ethanol in hippocampal slice from adult rat. J Neurosci. 1990;10(4):1372–9.

    PubMed  CAS  Google Scholar 

  105. Wirkner K et al. Mechanism of inhibition by ethanol of NMDA and AMPA receptor channel functions in cultured rat cortical neurons. Naunyn Schmiedebergs Arch Pharmacol. 2000;362(6):568–76.

    Article  PubMed  CAS  Google Scholar 

  106. Yin HH et al. Ethanol reverses the direction of long-term synaptic plasticity in the dorsomedial striatum. Eur J Neurosci. 2007;25(11):3226–32.

    Article  PubMed  Google Scholar 

  107. Kash TL, Matthews RT, Winder DG. Alcohol inhibits NR2B-containing NMDA receptors in the ventral bed nucleus of the stria terminalis. Neuropsychopharmacology. 2008;33(6):1379–90.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  108. Weitlauf C, Woodward JJ. Ethanol selectively attenuates NMDAR-mediated synaptic transmission in the prefrontal cortex. Alcohol Clin Exp Res. 2008;32(4):690–8.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  109. Di Chiara G, Imperato A. Ethanol preferentially stimulates dopamine release in the nucleus accumbens of freely moving rats. Eur J Pharmacol. 1985;115(1):131–2.

    Article  PubMed  Google Scholar 

  110. Robinson DL et al. Disparity between tonic and phasic ethanol-induced dopamine increases in the nucleus accumbens of rats. Alcohol Clin Exp Res. 2009;33(7):1187–96.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  111. Cho HS et al. Involvement of the endocannabinoid system in ethanol-induced corticostriatal synaptic depression. J Pharmacol Sci. 2012;120(1):45–9.

    Article  PubMed  CAS  Google Scholar 

  112. Lovinger DM, Kash TL. Mechanisms of neuroplasticity and ethanol’s effects on plasticity in the striatum and bed nucleus of the stria terminalis. Alcohol Res 2015; 37(1):109-24.

  113. 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.

  114. DePoy L et al. Chronic alcohol alters rewarded behaviors and striatal plasticity. Addict Biol. 2015;20(2):345–8.

    Article  PubMed  Google Scholar 

  115. Cuzon Carlson VC et al. Synaptic and morphological neuroadaptations in the putamen associated with long-term, relapsing alcohol drinking in primates. Neuropsychopharmacology. 2011;36(12):2513–28.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  116. Wilcox MV et al. Repeated binge-like ethanol drinking alters ethanol drinking patterns and depresses striatal GABAergic transmission. Neuropsychopharmacology. 2014;39(3):579–94.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  117. Siciliano CA et al. Voluntary ethanol intake predicts kappa-opioid receptor supersensitivity and regionally distinct dopaminergic adaptations in macaques. J Neurosci. 2015;35(15):5959–68.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  118. Cui SZ et al. Alteration of synaptic plasticity in rat dorsal striatum induced by chronic ethanol intake and withdrawal via ERK pathway. Acta Pharmacol Sin. 2011;32(2):175–81.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  119. Adermark L et al. Intermittent ethanol consumption depresses endocannabinoid-signaling in the dorsolateral striatum of rat. Neuropharmacology. 2011;61(7):1160–5.

    Article  PubMed  CAS  Google Scholar 

  120. Smith RJ, Aston-Jones G. Noradrenergic transmission in the extended amygdala: role in increased drug-seeking and relapse during protracted drug abstinence. Brain Struct Funct. 2008;213(1-2):43–61.

    Article  PubMed Central  PubMed  Google Scholar 

  121. McCool BA et al. Glutamate plasticity in the drunken amygdala: the making of an anxious synapse. Int Rev Neurobiol. 2010;91:205–33.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  122. Roberto M, Gilpin NW, Siggins GR. The central amygdala and alcohol: role of γ-aminobutyric acid, glutamate, and neuropeptides. Cold Spring Harb Perspect Med. 2012;2(12):a012195.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  123. Lack AK et al. Chronic ethanol and withdrawal effects on kainate receptor-mediated excitatory neurotransmission in the rat basolateral amygdala. Alcohol. 2009;43(1):25–33.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  124. Christian DT et al. Chronic intermittent ethanol and withdrawal differentially modulate basolateral amygdala AMPA-type glutamate receptor function and trafficking. Neuropharmacology. 2012;62(7):2430–9.

    Article  PubMed  CAS  Google Scholar 

  125. Diaz MR et al. Chronic ethanol and withdrawal differentially modulate lateral/basolateral amygdala paracapsular and local GABAergic synapses. J Pharmacol Exp Ther. 2011;337(1):162–70.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  126. Lindemeyer AK et al. Ethanol-induced plasticity of GABAA receptors in the basolateral amygdala. Neurochem Res. 2014;39(6):1162–70.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  127. Falco AM et al. Persisting changes in basolateral amygdala mRNAs after chronic ethanol consumption. Physiol Behav. 2009;96(1):169–73.

    Article  PubMed  CAS  Google Scholar 

  128. Trantham-Davidson H et al. Chronic alcohol disrupts dopamine receptor activity and the cognitive function of the medial prefrontal cortex. J Neurosci. 2014;34(10):3706–18.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  129. Koss WA et al. Effects of ethanol during adolescence on the number of neurons and glia in the medial prefrontal cortex and basolateral amygdala of adult male and female rats. Brain Res. 2012;1466:24–32.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  130. Kim A et al. Structural reorganization of pyramidal neurons in the medial prefrontal cortex of alcohol dependent rats is associated with altered glial plasticity. Brain Struct Funct. 2015;220(3):1705–20.

    Article  PubMed  CAS  Google Scholar 

  131. Vetreno RP, Crews FT. Adolescent binge drinking increases expression of the danger signal receptor agonist HMGB1 and Toll-like receptors in the adult prefrontal cortex. Neuroscience. 2012;226:475–88.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  132. Liu W, Crews F. Adolescent Intermittent ethanol exposure enhances ethanol activation of the nucleus accumbens while blunting the prefrontal cortex responses in adult rat. Neuroscience. 2015;293:92–108.

    Article  PubMed  CAS  Google Scholar 

  133. Acosta G et al. Ethanol self-administration modulation of NMDA receptor subunit and related synaptic protein mRNA expression in prefrontal cortical fields in cynomolgus monkeys. Brain Res. 2010;1318:144–54.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  134. Hemby SE et al. Ethanol-induced regulation of GABA-A subunit mRNAs in prefrontal fields of cynomolgus monkeys. Alcohol Clin Exp Res. 2006;30(12):1978–85.

    Article  PubMed  CAS  Google Scholar 

  135. Kroenke CD et al. Monkeys that voluntarily and chronically drink alcohol damage their brains: a longitudinal MRI study. Neuropsychopharmacology. 2014;39(4):823–30.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  136. Bjork JM, Gilman JM. The effects of acute alcohol administration on the human brain: insights from neuroimaging. Neuropharmacology. 2014;84:101–10.

    Article  PubMed  CAS  Google Scholar 

  137. Zoethout RW et al. Functional biomarkers for the acute effects of alcohol on the central nervous system in healthy volunteers. Br J Clin Pharmacol. 2011;71(3):331–50.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  138. Yoder KK et al. Heterogeneous effects of alcohol on dopamine release in the striatum: a PET study. Alcohol Clin Exp Res. 2007;31(6):965–73.

    Article  PubMed  CAS  Google Scholar 

  139. Mitchell JM et al. Alcohol consumption induces endogenous opioid release in the human orbitofrontal cortex and nucleus accumbens. Sci Transl Med. 2012;4(116):116ra6.

    Article  PubMed  CAS  Google Scholar 

  140. Vetreno RP, Qin L, Crews FT. Increased receptor for advanced glycation end product expression in the human alcoholic prefrontal cortex is linked to adolescent drinking. Neurobiol Dis. 2013;59:52–62.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  141. Koob GF. Negative reinforcement in drug addiction: the darkness within. Curr Opin Neurobiol. 2013;23(4):559–63.

    Article  PubMed  CAS  Google Scholar 

  142. Koob GF. Theoretical frameworks and mechanistic aspects of alcohol addiction: alcohol addiction as a reward deficit disorder. Curr Top Behav Neurosci. 2013;13:3–30.

    Article  PubMed Central  PubMed  Google Scholar 

  143. Yin HH. From actions to habits: neuroadaptations leading to dependence. Alcohol Res Health. 2008;31(4):340–4.

    PubMed Central  PubMed  Google Scholar 

  144. Barker JM, Taylor JR. Habitual alcohol seeking: modeling the transition from casual drinking to addiction. Neurosci Biobehav Rev. 2014;47:281–94.

    Article  PubMed  CAS  Google Scholar 

  145. O’Tousa D, Grahame N. Habit formation: implications for alcoholism research. Alcohol. 2014;48(4):327–35.

    Article  PubMed Central  PubMed  Google Scholar 

  146. Barker JM, et al. Corticostriatal circuitry and habitual ethanol seeking. Alcohol. 2015;49(8):817–824.

  147. Dickinson A, Wood N, Smith JW. Alcohol seeking by rats: action or habit? Q J Exp Psychol B. 2002;55(4):331–48.

    Article  PubMed  Google Scholar 

  148. Samson HH et al. Devaluation of ethanol reinforcement. Alcohol. 2004;32(3):203–12.

    Article  PubMed  CAS  Google Scholar 

  149. 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(7):639–45.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  150. Hogarth L et al. Acute alcohol impairs human goal-directed action. Biol Psychol. 2012;90(2):154–60. Human laboratory study that demonstrates actue alcohol administration can change choice behavior for food (chocolate) reward.

    Article  PubMed  Google Scholar 

  151. Sebold M et al. Model-based and model-free decisions in alcohol dependence. Neuropsychobiology. 2014;70(2):122–31.

    Article  PubMed  CAS  Google Scholar 

  152. Muskens JB et al. Damage in the dorsal striatum alleviates addictive behavior. Gen Hosp Psychiatry. 2012;34(6):702. e9-702 e11.

    Article  PubMed  Google Scholar 

  153. Gillan CM et al. Enhanced avoidance habits in obsessive-compulsive disorder. Biol Psychiatry. 2014;75(8):631–8.

    Article  PubMed Central  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Psychology and Neuroscience, University of North Carolina at Chapel Hill, Davie Hall, CB #3270, Chapel Hill, NC, 27599, USA

    Theresa H. McKim

  2. Bowles Center for Alcohol Studies, University of North Carolina at Chapel Hill, CB #7178, Chapel Hill, NC, 27599, USA

    Tatiana A. Shnitko

  3. Department of Psychiatry, Bowles Center for Alcohol Studies, University of North Carolina at Chapel Hill, CB #7178, Chapel Hill, NC, 27599, USA

    Donita L. Robinson

  4. Department of Psychology and Neuroscience, Biomedical Research Imaging Center, Bowles Center for Alcohol Studies, University of North Carolina at Chapel Hill, Davie Hall, CB #3270, Chapel Hill, NC, 27599, USA

    Charlotte A. Boettiger

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  1. Theresa H. McKim
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  2. Tatiana A. Shnitko
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  3. Donita L. Robinson
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  4. Charlotte A. Boettiger
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Correspondence to Donita L. Robinson or Charlotte A. Boettiger.

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Conflict of Interest

Charlotte A. Boettiger receives consulting fees from BlackThorn Therapeutics, Inc.

Donita L. Robinson declares no conflict of interest.

Theresa H. McKim declares no conflict of interest.

Tatiana Shnitko declares no conflict of interest.

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This article does not contain any studies with human or animal subjects performed by any of the authors.

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This article is part of the Topical Collection on Alcohol

Theresa H. McKim and Tatiana A. Shnitko are co-first authors

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McKim, T.H., Shnitko, T.A., Robinson, D.L. et al. Translational Research on Habit and Alcohol. Curr Addict Rep 3, 37–49 (2016). https://doi.org/10.1007/s40429-016-0089-8

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