Advertisement

Alcohol Effects on the Dorsal Striatum

  • Mary H. Patton
  • Aparna P. Shah
  • Brian N. MathurEmail author
Chapter
Part of the Innovations in Cognitive Neuroscience book series (Innovations Cogn.Neuroscience)

Abstract

The dorsal striatum is involved in action learning/selection. Distinguishable forms of action learning, goal-directed and habitual learning, are mediated by medial and lateral subdivisions of the dorsal striatum, respectively. Data from several studies now support the emerging picture that alcohol remodels dorsal striatal macro- and microcircuitry to promote the expression of habitual action strategies. In this chapter, we review known alcohol effects on the various synapse and cell types of the dorsal striatum and synthesize this work with what is known about alcohol’s influence on striatal-mediated behaviors. We conclude with a discussion of how alcohol action on dorsal striatum physiology may foster compulsive drinking, a hallmark of alcoholism.

Keywords

Alcohol abuse Striatum Habits Neuronal plasticity 

References

  1. Adams CD (1982) Variations in the sensitivity of instrumental responding to reinforcer devaluation. Q J Exp Psychol Sect B Comp Physiol Psychol 34(2):77–98Google Scholar
  2. Adermark L, Lovinger DM (2007a) Combined activation of L-type Ca2+ channels and synaptic transmission is sufficient to induce striatal long-term depression. J Neurosci 27(25):6781–6787. doi: 10.1523/JNEUROSCI.0280-07.2007 PubMedCrossRefGoogle Scholar
  3. Adermark L, Lovinger DM (2007b) Retrograde endocannabinoid signaling at striatal synapses requires a regulated postsynaptic release step. Proc Natl Acad Sci U S A 104(51):20564–20569. doi: 10.1073/pnas.0706873104 PubMedPubMedCentralCrossRefGoogle Scholar
  4. Adermark L, Talani G, Lovinger DM (2009) Endocannabinoid-dependent plasticity at GABAergic and glutamatergic synapses in the striatum is regulated by synaptic activity. Eur J Neurosci 29(1):32–41. doi: 10.1111/j.1460-9568.2008.06551.x PubMedPubMedCentralCrossRefGoogle Scholar
  5. Adermark L, Clarke RB, Soderpalm B, Ericson M (2011a) Ethanol-induced modulation of synaptic output from the dorsolateral striatum in rat is regulated by cholinergic interneurons. Neurochem Int 58(6):693–699. doi: 10.1016/j.neuint.2011.02.009 PubMedCrossRefGoogle Scholar
  6. Adermark L, Jonsson S, Ericson M, Soderpalm B (2011b) Intermittent ethanol consumption depresses endocannabinoid-signaling in the dorsolateral striatum of rat. Neuropharmacology 61(7):1160–1165. doi: 10.1016/j.neuropharm.2011.01.014 PubMedCrossRefGoogle Scholar
  7. Adermark L, Jonsson S, Soderpalm B, Ericson M (2013) Region-specific depression of striatal activity in Wistar rat by modest ethanol consumption over a ten-month period. Alcohol 47(4):289–298. doi: 10.1016/j.alcohol.2013.03.003 PubMedCrossRefGoogle Scholar
  8. Aosaki T, Tsubokawa H, Ishida A et al (1994) Responses of tonically active neurons in the primate’s striatum undergo systematic changes during behavioral sensorimotor conditioning. J Neurosci 14(6):3969–3984PubMedGoogle Scholar
  9. Atwood BK, Lovinger DM, Mathur BN (2014) Presynaptic long-term depression mediated by Gi/o-coupled receptors. Trends Neurosci 37(11):663–673. doi: 10.1016/j.tins.2014.07.010 PubMedPubMedCentralCrossRefGoogle Scholar
  10. Barkley-Levenson AM, Crabbe JC (2014) High drinking in the dark mice: a genetic model of drinking to intoxication. Alcohol 48(3):217–223. doi: 10.1016/j.alcohol.2013.10.007 PubMedCrossRefGoogle Scholar
  11. Barnes TD, Kubota Y, Hu D, Jin DZ, Graybiel AM (2005) Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories. Nature 437(7062):1158–1161. doi: 10.1038/nature04053 PubMedCrossRefGoogle Scholar
  12. Barr CS, Goldman D (2006) Non-human primate models of inheritance vulnerability to alcohol use disorders. Addict Biol 11(3-4):374–385. doi: 10.1111/j.1369-1600.2005.00034.x PubMedCrossRefGoogle Scholar
  13. Basavarajappa BS, Ninan I, Arancio O (2008) Acute ethanol suppresses glutamatergic neurotransmission through endocannabinoids in hippocampal neurons. J Neurochem 107(4):1001–1013. doi: 10.1111/j.1471-4159.2008.05685.x PubMedPubMedCentralGoogle Scholar
  14. Becker HC (2013) Animal models of excessive alcohol consumption in rodents. Curr Top Behav Neurosci 13:355–377. doi: 10.1007/7854_2012_203 PubMedCrossRefGoogle Scholar
  15. Becker HC, Ron D (2014) Animal models of excessive alcohol consumption: recent advances and future challenges. Alcohol 48(3):205–208. doi: 10.1016/j.alcohol.2014.04.001 PubMedPubMedCentralCrossRefGoogle Scholar
  16. Bell RL, Rodd ZA, Engleman EA et al (2014) Scheduled access alcohol drinking by alcohol-preferring (P) and high-alcohol-drinking (HAD) rats: modeling adolescent and adult binge-like drinking. Alcohol 48(3):225–234. doi: 10.1016/j.alcohol.2013.10.004 PubMedCrossRefGoogle Scholar
  17. Benhamou L, Kehat O, Cohen D (2014) Firing pattern characteristics of tonically active neurons in rat striatum: context dependent or species divergent? J Neurosci 34(6):2299–2304. doi: 10.1523/JNEUROSCI.1798-13.2014 PubMedCrossRefGoogle Scholar
  18. Blomeley CP, Cains S, Smith R, Bracci E (2011) Ethanol affects striatal interneurons directly and projection neurons through a reduction in cholinergic tone. Neuropsychopharmacology 36(5):1033–1046. doi: 10.1038/npp.2010.241 PubMedPubMedCentralCrossRefGoogle Scholar
  19. Calabresi P, Maj R, Pisani A et al (1992a) Long-term synaptic depression in the striatum: physiological and pharmacological characterization. J Neurosci 12(11):4224–4233PubMedGoogle Scholar
  20. Calabresi P, Pisani A, Mercuri NB et al (1992b) Long-term potentiation in the striatum is unmasked by removing the voltage-dependent magnesium block of NMDA receptor channels. Eur J Neurosci 4(10):929–935PubMedCrossRefGoogle Scholar
  21. Carnicella S, Ron D, Barak S (2014) Intermittent ethanol access schedule in rats as a preclinical model of alcohol abuse. Alcohol 48(3):243–252. doi: 10.1016/j.alcohol.2014.01.006 PubMedPubMedCentralCrossRefGoogle Scholar
  22. Carta M, Mameli M, Valenzuela CF (2004) Alcohol enhances GABAergic transmission to cerebellar granule cells via an increase in Golgi cell excitability. J Neurosci 24(15):3746–3751. doi: 10.1523/JNEUROSCI.0067-04.2004 PubMedCrossRefGoogle Scholar
  23. Chen G, Cuzon Carlson VC, Wang J et al (2011) Striatal involvement in human alcoholism and alcohol consumption, and withdrawal in animal models. Alcohol Clin Exp Res 35(10):1739–1748. doi: 10.1111/j.1530-0277.2011.01520.x PubMedPubMedCentralCrossRefGoogle Scholar
  24. Choi SJ, Kim KJ, Cho HS et al (2006) Acute inhibition of corticostriatal synaptic transmission in the rat dorsal striatum by ethanol. Alcohol 40(2):95–101. doi: 10.1016/j.alcohol.2006.12.004 PubMedCrossRefGoogle Scholar
  25. Clarke RB, Adermark L (2010) Acute ethanol treatment prevents endocannabinoid-mediated long-lasting disinhibition of striatal output. Neuropharmacology 58(4-5):799–805. doi: 10.1016/j.neuropharm.2009.12.006 PubMedCrossRefGoogle Scholar
  26. Colombo G, Maccioni P, Acciaro C et al (2014) Binge drinking in alcohol-preferring sP rats at the end of the nocturnal period. Alcohol 48(3):301–311. doi: 10.1016/j.alcohol.2014.02.001 PubMedPubMedCentralCrossRefGoogle Scholar
  27. Corbit LH, Nie H, Janak PH (2012) Habitual alcohol seeking: time course and the contribution of subregions of the dorsal striatum. Biol Psychiatry 72(5):389–395. doi: 10.1016/j.biopsych.2012.02.024 PubMedPubMedCentralCrossRefGoogle Scholar
  28. Corbit LH, Nie H, Janak PH (2014) Habitual responding for alcohol depends upon both AMPA and D2 receptor signaling in the dorsolateral striatum. Front Behav Neurosci 8:301. doi: 10.3389/fnbeh.2014.00301 PubMedPubMedCentralCrossRefGoogle Scholar
  29. Coutureau E, Killcross S (2003) Inactivation of the infralimbic prefrontal cortex reinstates goal-directed responding in overtrained rats. Behav Brain Res 146(1-2):167–174PubMedCrossRefGoogle Scholar
  30. Cui SZ, Wang SJ, Li J et al (2011) Alteration of synaptic plasticity in rat dorsal striatum induced by chronic ethanol intake and withdrawal via ERK pathway. Acta Pharmacol Sin 32(2):175–181. doi: 10.1038/aps.2010.199 PubMedPubMedCentralCrossRefGoogle Scholar
  31. Cuzon Carlson VC, Seabold GK, Helms CM et al (2011) Synaptic and morphological neuroadaptations in the putamen associated with long-term, relapsing alcohol drinking in primates. Neuropsychopharmacology 36(12):2513–2528. doi: 10.1038/npp.2011.140 PubMedPubMedCentralCrossRefGoogle Scholar
  32. de Rover M, Lodder JC, Kits KS et al (2002) Cholinergic modulation of nucleus accumbens medium spiny neurons. Eur J Neurosci 16(12):2279–2290PubMedCrossRefGoogle Scholar
  33. Deitrich RA, Erwin VG (1996) Pharmacological effects of ethanol on the nervous system. Pharmacology and toxicology. CRC Press, Boca RatonGoogle Scholar
  34. DePoy L, Daut R, Brigman JL et al (2013) Chronic alcohol produces neuroadaptations to prime dorsal striatal learning. Proc Natl Acad Sci U S A 110(36):14783–14788. doi: 10.1073/pnas.1308198110 PubMedPubMedCentralCrossRefGoogle Scholar
  35. DePoy L, Daut R, Wright T et al (2015) Chronic alcohol alters rewarded behaviors and striatal plasticity. Addict Biol 20(2):345–348. doi: 10.1111/adb.12131 PubMedCrossRefGoogle Scholar
  36. Dezfouli A, Balleine BW (2012) Habits, action sequences and reinforcement learning. Eur J Neurosci 35(7):1036–1051. doi: 10.1111/j.1460-9568.2012.08050.x PubMedPubMedCentralCrossRefGoogle Scholar
  37. Dickinson A, Wood N, Smith JW (2002) Alcohol seeking by rats: action or habit? Q J Exp Psychol B 55(4):331–348. doi: 10.1080/0272499024400016 PubMedCrossRefGoogle Scholar
  38. Ding JB, Guzman JN, Peterson JD et al (2010) Thalamic gating of corticostriatal signaling by cholinergic interneurons. Neuron 67(2):294–307. doi: 10.1016/j.neuron.2010.06.017 PubMedPubMedCentralCrossRefGoogle Scholar
  39. Edwards G, Gross MM (1976) Alcohol dependence: provisional description of a clinical syndrome. Br Med J 1(6017):1058–1061PubMedPubMedCentralCrossRefGoogle Scholar
  40. English JD, Sweatt JD (1997) A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J Biol Chem 272(31):19103–19106PubMedCrossRefGoogle Scholar
  41. Fachin-Scheit DJ, Frozino Ribeiro A, Pigatto G et al (2006) Development of a mouse model of ethanol addiction: naltrexone efficacy in reducing consumption but not craving. J Neural Transm 113(9):1305–1321. doi: 10.1007/s00702-005-0416-z PubMedCrossRefGoogle Scholar
  42. Fanelli RR, Klein JT, Reese RM et al (2013) Dorsomedial and dorsolateral striatum exhibit distinct phasic neuronal activity during alcohol self-administration in rats. Eur J Neurosci 38(4):2637–2648. doi: 10.1111/ejn.12271 PubMedPubMedCentralCrossRefGoogle Scholar
  43. Faure A, Haberland U, Conde F et al (2005) Lesion to the nigrostriatal dopamine system disrupts stimulus-response habit formation. J Neurosci 25(11):2771–2780. doi: 10.1523/JNEUROSCI.3894-04.2005 PubMedCrossRefGoogle Scholar
  44. Ford MM (2014) Applications of schedule-induced polydipsia in rodents for the study of an excessive ethanol intake phenotype. Alcohol 48(3):265–276. doi: 10.1016/j.alcohol.2014.01.005 PubMedPubMedCentralCrossRefGoogle Scholar
  45. Fu L, Beckstead RM (1992) Cortical stimulation induces fos expression in striatal neurons. Neuroscience 46(2):329–334PubMedCrossRefGoogle Scholar
  46. Gasbarri A, Pompili A, Packard MG et al (2014) Habit learning and memory in mammals: behavioral and neural characteristics. Neurobiol Learn Mem 114:198–208. doi: 10.1016/j.nlm.2014.06.010 PubMedCrossRefGoogle Scholar
  47. Gerdeman GL, Ronesi J, Lovinger DM (2002) Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat Neurosci 5(5):446–451. doi: 10.1038/nn832 PubMedGoogle Scholar
  48. Gerdeman GL, Partridge JG, Lupica CR et al (2003) It could be habit forming: drugs of abuse and striatal synaptic plasticity. Trends Neurosci 26(4):184–192. doi: 10.1016/S0166-2236(03)00065-1 PubMedCrossRefGoogle Scholar
  49. Gittis AH, Nelson AB, Thwin MT et al (2010) Distinct roles of GABAergic interneurons in the regulation of striatal output pathways. J Neurosci 30(6):2223–2234. doi: 10.1523/JNEUROSCI.4870-09.2010 PubMedPubMedCentralCrossRefGoogle Scholar
  50. Grant KA, Leng X, Green HL et al (2008) Drinking typography established by scheduled induction predicts chronic heavy drinking in a monkey model of ethanol self-administration. Alcohol Clin Exp Res 32(10):1824–1838. doi: 10.1111/j.1530-0277.2008.00765.x PubMedPubMedCentralCrossRefGoogle Scholar
  51. Gremel CM, Costa RM (2013) Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual actions. Nat Commun 4:2264. doi: 10.1038/ncomms3264 PubMedPubMedCentralCrossRefGoogle Scholar
  52. Griffin WC III (2014) Alcohol dependence and free-choice drinking in mice. Alcohol 48(3):287–293. doi: 10.1016/j.alcohol.2013.11.006 PubMedPubMedCentralCrossRefGoogle Scholar
  53. Hardingham GE, Arnold FJ, Bading H (2001) A calcium microdomain near NMDA receptors: on switch for ERK-dependent synapse-to-nucleus communication. Nat Neurosci 4(6):565–566. doi: 10.1038/88380 PubMedCrossRefGoogle Scholar
  54. Hart G, Leung BK, Balleine BW (2014) Dorsal and ventral streams: the distinct role of striatal subregions in the acquisition and performance of goal-directed actions. Neurobiol Learn Mem 108:104–118. doi: 10.1016/j.nlm.2013.11.003 PubMedCrossRefGoogle Scholar
  55. Herrero MT, Barcia C, Navarro JM (2002) Functional anatomy of thalamus and basal ganglia. Childs Nerv Syst 18(8):386–404. doi: 10.1007/s00381-002-0604-1 PubMedCrossRefGoogle Scholar
  56. Hill MN, Hillard CJ, McEwen BS (2011) Alterations in corticolimbic dendritic morphology and emotional behavior in cannabinoid CB1 receptor-deficient mice parallel the effects of chronic stress. Cereb Cortex 21(9):2056–2064. doi: 10.1093/cercor/bhq280 PubMedPubMedCentralCrossRefGoogle Scholar
  57. Hopf FW, Lesscher HMB (2014) Rodent models for compulsive alcohol intake. Alcohol 48(3):253–264. doi: 10.1016/j.alcohol.2014.03.001 PubMedPubMedCentralCrossRefGoogle Scholar
  58. Izumi Y, Nagashima K, Murayama K et al (2005) Acute effects of ethanol on hippocampal long-term potentiation and long-term depression are mediated by different mechanisms. Neuroscience 136(2):509–517. doi: 10.1016/j.neuroscience.2005.08.002 PubMedCrossRefGoogle Scholar
  59. Jeanblanc J, He DY, Carnicella S et al (2009) Endogenous BDNF in the dorsolateral striatum gates alcohol drinking. J Neurosci 29(43):13494–13502. doi: 10.1523/JNEUROSCI.2243-09.2009 PubMedPubMedCentralCrossRefGoogle Scholar
  60. Kawaguchi Y (1993) Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 13(11):4908–4923PubMedGoogle Scholar
  61. Kelm MK, Criswell HE, Breese GR (2011) Ethanol-enhanced GABA release: a focus on G protein-coupled receptors. Brain Res Rev 65(2):113–123. doi: 10.1016/j.brainresrev.2010.09.003 PubMedCrossRefGoogle Scholar
  62. Killcross S, Coutureau E (2003) Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb Cortex 13(4):400–408PubMedCrossRefGoogle Scholar
  63. Kimura M, Rajkowski J, Evarts E (1984) Tonically discharging putamen neurons exhibit set-dependent responses. Proc Natl Acad Sci U S A 81(15):4998–5001PubMedPubMedCentralCrossRefGoogle Scholar
  64. Knowlton BJ, Mangels JA, Squire LR (1996) A neostriatal habit learning system in humans. Science 273(5280):1399–1402PubMedCrossRefGoogle Scholar
  65. Krystal JH, Petrakis IL, Mason G et al (2003) N-methyl-D-aspartate glutamate receptors and alcoholism: reward, dependence, treatment, and vulnerability. Pharmacol Ther 99(1):79–94PubMedCrossRefGoogle Scholar
  66. Lesscher HM, van Kerkhof LW, Vanderschuren LJ (2010) Inflexible and indifferent alcohol drinking in male mice. Alcohol Clin Exp Res 34(7):1219–1225. doi: 10.1111/j.1530-0277.2010.01199.x PubMedGoogle Scholar
  67. Li Q, Wilson WA, Swartzwelder HS (2006) Developmental differences in the sensitivity of spontaneous and miniature IPSCs to ethanol. Alcohol Clin Exp Res 30(1):119–126. doi: 10.1111/j.1530-0277.2006.00006.x PubMedCrossRefGoogle Scholar
  68. Lopez MF, Becker HC (2014) Operant ethanol self-administration in ethanol dependent mice. Alcohol 48(3):295–299. doi: 10.1016/j.alcohol.2014.02.002 PubMedPubMedCentralCrossRefGoogle Scholar
  69. Lovinger DM, Mathur BN (2012) Endocannabinoids in striatal plasticity. Parkinsonism Relat Disord 18(Suppl 1):S132–S134. doi: 10.1016/S1353-8020(11)70041-4 PubMedPubMedCentralCrossRefGoogle Scholar
  70. Lovinger DM, Roberto M (2013) Synaptic effects induced by alcohol. Curr Top Behav Neurosci 13:31–86. doi: 10.1007/7854_2011_143 PubMedPubMedCentralCrossRefGoogle Scholar
  71. Lovinger DM, White G, Weight FF (1989) Ethanol inhibits NMDA-activated ion current in hippocampal neurons. Science 243(4899):1721–1724PubMedCrossRefGoogle Scholar
  72. Lovinger DM, Tyler EC, Merritt A (1993) Short- and long-term synaptic depression in rat neostriatum. J Neurophysiol 70(5):1937–1949PubMedGoogle Scholar
  73. Malenka RC, Nicoll RA (1999) Long-term potentiation—a decade of progress? Science 285(5435):1870–1874PubMedCrossRefGoogle Scholar
  74. Mallet N, Le Moine C, Charpier S et al (2005) Feedforward inhibition of projection neurons by fast-spiking GABA interneurons in the rat striatum in vivo. J Neurosci 25(15):3857–3869. doi: 10.1523/JNEUROSCI.5027-04.2005 Google Scholar
  75. Martin SJ, Grimwood PD, Morris RG (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649–711. doi: 10.1146/annurev.neuro.23.1.649 PubMedCrossRefGoogle Scholar
  76. Mathur BN, Tanahira C, Tamamaki N et al (2013) Voltage drives diverse endocannabinoid signals to mediate striatal microcircuit-specific plasticity. Nat Neurosci 16(9):1275–1283. doi: 10.1038/nn.3478 PubMedPubMedCentralCrossRefGoogle Scholar
  77. McBride WJ, Rodd ZA, Bell RL et al (2014) The alcohol-preferring (P) and high-alcohol-drinking (HAD) rats—animal models of alcoholism. Alcohol 48(3):209–215. doi: 10.1016/j.alcohol.2013.09.044 PubMedCrossRefGoogle Scholar
  78. Melis M, Camarini R, Ungless MA et al (2002) Long-lasting potentiation of GABAergic synapses in dopamine neurons after a single in vivo ethanol exposure. J Neurosci 22(6):2074–2082PubMedGoogle Scholar
  79. Morrisett RA, Swartzwelder HS (1993) Attenuation of hippocampal long-term potentiation by ethanol: a patch-clamp analysis of glutamatergic and GABAergic mechanisms. J Neurosci 13(5):2264–2272PubMedGoogle Scholar
  80. Nam HW, Hinton DJ, Kang NY et al (2013) Adenosine transporter ENT1 regulates the acquisition of goal-directed behavior and ethanol drinking through A2A receptor in the dorsomedial striatum. J Neurosci 33(10):4329–4338. doi: 10.1523/JNEUROSCI.3094-12.2013 PubMedPubMedCentralCrossRefGoogle Scholar
  81. Nie Z, Yuan X, Madamba SG et al (1993) Ethanol decreases glutamatergic synaptic transmission in rat nucleus accumbens in vitro: naloxone reversal. J Pharmacol Exp Ther 266(3):1705–1712PubMedGoogle Scholar
  82. Nie Z, Madamba SG, Siggins GR (1994) Ethanol inhibits glutamatergic neurotransmission in nucleus accumbens neurons by multiple mechanisms. J Pharmacol Exp Ther 271(3):1566–1573PubMedGoogle Scholar
  83. Nielsen CK, Simms JA, Li R et al (2012) Delta-opioid receptor function in the dorsal striatum plays a role in high levels of ethanol consumption in rats. J Neurosci 32(13):4540–4552. doi: 10.1523/JNEUROSCI.5345-11.2012 PubMedCrossRefGoogle Scholar
  84. Oldenburg IA, Ding JB (2011) Cholinergic modulation of synaptic integration and dendritic excitability in the striatum. Curr Opin Neurobiol 21(3):425–432. doi: 10.1016/j.conb.2011.04.004 PubMedPubMedCentralCrossRefGoogle Scholar
  85. Packard MG (1999) Glutamate infused posttraining into the hippocampus or caudate-putamen differentially strengthens place and response learning. Proc Natl Acad Sci U S A 96(22):12881–12886PubMedPubMedCentralCrossRefGoogle Scholar
  86. Packard MG, McGaugh JL (1992) Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: further evidence for multiple memory systems. Behav Neurosci 106(3):439–446PubMedCrossRefGoogle Scholar
  87. Packard MG, McGaugh JL (1996) Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol Learn Mem 65(1):65–72. doi: 10.1006/nlme.1996.0007 PubMedCrossRefGoogle Scholar
  88. Packard MG, Hirsh R, White NM (1989) Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems. J Neurosci 9(5):1465–1472PubMedGoogle Scholar
  89. Partridge JG, Tang KC, Lovinger DM (2000) Regional and postnatal heterogeneity of activity-dependent long-term changes in synaptic efficacy in the dorsal striatum. J Neurophysiol 84(3):1422–1429PubMedGoogle Scholar
  90. Partridge JG, Apparsundaram S, Gerhardt GA et al (2002) Nicotinic acetylcholine receptors interact with dopamine in induction of striatal long-term depression. J Neurosci 22(7):2541–2549. doi:20026219PubMedGoogle Scholar
  91. Perra S, Pillolla G, Luchicchi A et al (2008) Alcohol inhibits spontaneous activity of basolateral amygdala projection neurons in the rat: involvement of the endocannabinoid system. Alcohol Clin Exp Res 32(3):443–449. doi: 10.1111/j.1530-0277.2007.00588.x PubMedCrossRefGoogle Scholar
  92. Pisani A, Bernardi G, Ding J, Surmeier DJ (2007) Re-emergence of striatal cholinergic interneurons in movement disorders. Trends Neurosci 30(10):545–553. doi: 10.1016/j.tins.2007.07.008 PubMedCrossRefGoogle Scholar
  93. Patton MH, Roberts BM, Lovinger DM, Mathur BN. (2016) Ethanol Disinhibits Dorsolateral Striatal Medium Spiny Neurons Through Activation of A Presynaptic Delta Opioid Receptor. Neuropsychopharmacology 41(7):1831–1840. doi: 10.1038/npp.2015.353 Google Scholar
  94. Quinn JJ, Pittenger C, Lee AS et al (2013) Striatum-dependent habits are insensitive to both increases and decreases in reinforcer value in mice. Eur J Neurosci 37(6):1012–1021. doi: 10.1111/ejn.12106 PubMedPubMedCentralCrossRefGoogle Scholar
  95. Rhodes JS, Best K, Belknap JK et al (2005) Evaluation of a simple model of ethanol drinking to intoxication in C57BL/6J mice. Physiol Behav 84(1):53–63. doi: 10.1016/j.physbeh.2004.10.007 PubMedCrossRefGoogle Scholar
  96. Rhodes JS, Ford MM, Yu CH et al (2007) Mouse inbred strain differences in ethanol drinking to intoxication. Genes Brain Behav 6(1):1–18. doi: 10.1111/j.1601-183X.2006.00210.x PubMedCrossRefGoogle Scholar
  97. Robbins TW, Everitt BJ (2002) Limbic-striatal memory systems and drug addiction. Neurobiol Learn Mem 78(3):625–636PubMedCrossRefGoogle Scholar
  98. Roberto M, Madamba SG, Moore SD et al (2003) Ethanol increases GABAergic transmission at both pre- and postsynaptic sites in rat central amygdala neurons. Proc Natl Acad Sci U S A 100(4):2053–2058. doi: 10.1073/pnas.0437926100 PubMedPubMedCentralCrossRefGoogle Scholar
  99. Rolls ET (1994) Neurophysiology and cognitive functions of the striatum. Rev Neurol (Paris) 150(8-9):648–660Google Scholar
  100. Ron D, Wang J (2009) The NMDA receptor and alcohol addiction. In: Van Dongen AM (ed) Biology of the NMDA receptor. Frontiers in neuroscience. CRC Press, Boca RatonGoogle Scholar
  101. Rosenblum K, Futter M, Voss K et al (2002) The role of extracellular regulated kinases I/II in late-phase long-term potentiation. J Neurosci 22(13):5432–5441. doi:20026549PubMedGoogle Scholar
  102. Samson HH, Pfeffer AO (1987) Initiation of ethanol-maintained responding using a schedule-induction procedure in free feeding rats. Alcohol Drug Res 7(5-6):461–469PubMedGoogle Scholar
  103. Schummers J, Bentz S, Browning MD (1997) Ethanol’s inhibition of LTP may not be mediated solely via direct effects on the NMDA receptor. Alcohol Clin Exp Res 21(3):404–408PubMedCrossRefGoogle Scholar
  104. Sesack SR, Deutch AY, Roth RH et al (1989) Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J Comp Neurol 290(2):213–242. doi: 10.1002/cne.902900205 PubMedCrossRefGoogle Scholar
  105. Shen W, Tian X, Day M et al (2007) Cholinergic modulation of Kir2 channels selectively elevates dendritic excitability in striatopallidal neurons. Nat Neurosci 10(11):1458–1466. doi: 10.1038/nn1972 PubMedCrossRefGoogle Scholar
  106. Shen W, Flajolet M, Greengard P et al (2008) Dichotomous dopaminergic control of striatal synaptic plasticity. Science 321(5890):848–851. doi: 10.1126/science.1160575 PubMedPubMedCentralCrossRefGoogle Scholar
  107. Sjoerds Z, de Wit S, van den Brink W et al (2013) Behavioral and neuroimaging evidence for overreliance on habit learning in alcohol-dependent patients. Transl Psychiatry 3:e337. doi: 10.1038/tp.2013.107 PubMedPubMedCentralCrossRefGoogle Scholar
  108. Thiele TE, Navarro M (2014) “Drinking in the dark” (DID) procedures: a model of binge-like ethanol drinking in non-dependent mice. Alcohol 48(3):235–241. doi: 10.1016/j.alcohol.2013.08.005 PubMedCrossRefGoogle Scholar
  109. Uchigashima M, Narushima M, Fukaya M et al (2007) Subcellular arrangement of molecules for 2-arachidonoyl-glycerol-mediated retrograde signaling and its physiological contribution to synaptic modulation in the striatum. J Neurosci 27(14):3663–3676. doi: 10.1523/JNEUROSCI.0448-07.2007 PubMedCrossRefGoogle Scholar
  110. Valenzuela CF (1997) Alcohol and neurotransmitter interactions. Alcohol Health Res World 21(2):144–148PubMedGoogle Scholar
  111. Vendruscolo LF, Roberts AJ (2014) Operant alcohol self-administration in dependent rats: focus on the vapor model. Alcohol 48(3):277–286. doi: 10.1016/j.alcohol.2013.08.006 PubMedCrossRefGoogle Scholar
  112. Vengeliene V, Bilbao A, Spanagel R (2014) The alcohol deprivation effect model for studying relapse behavior: a comparison between rats and mice. Alcohol 48(3):313–320. doi: 10.1016/j.alcohol.2014.03.002 PubMedCrossRefGoogle Scholar
  113. Vivian JA, Green HL, Young JE et al (2001) Induction and maintenance of ethanol self-administration in cynomolgus monkeys (Macaca fascicularis): long-term characterization of sex and individual differences. Alcohol Clin Exp Res 25(8):1087–1097PubMedCrossRefGoogle Scholar
  114. Vollstadt-Klein S, Wichert S, Rabinstein J et al (2010) Initial, habitual and compulsive alcohol use is characterized by a shift of cue processing from ventral to dorsal striatum. Addiction 105(10):1741–1749. doi: 10.1111/j.1360-0443.2010.03022.x PubMedCrossRefGoogle Scholar
  115. Wan XS, Liang F, Moret V et al (1992) Mapping of the motor pathways in rats: c-fos induction by intracortical microstimulation of the motor cortex correlated with efferent connectivity of the site of cortical stimulation. Neuroscience 49(4):749–761PubMedCrossRefGoogle Scholar
  116. Wang Z, Kai L, Day M, Ronesi J et al (2006) Dopaminergic control of corticostriatal long-term synaptic depression in medium spiny neurons is mediated by cholinergic interneurons. Neuron 50(3):443–452. doi: 10.1016/j.neuron.2006.04.010 PubMedCrossRefGoogle Scholar
  117. Wang J, Carnicella S, Phamluong K et al (2007) Ethanol induces long-term facilitation of NR2B-NMDA receptor activity in the dorsal striatum: implications for alcohol drinking behavior. J Neurosci 27(13):3593–3602. doi: 10.1523/JNEUROSCI.4749-06.2007 PubMedCrossRefGoogle Scholar
  118. Wang J, Lanfranco MF, Gibb SL et al (2010) Long-lasting adaptations of the NR2B-containing NMDA receptors in the dorsomedial striatum play a crucial role in alcohol consumption and relapse. J Neurosci 30(30):10187–10198. doi: 10.1523/JNEUROSCI.2268-10.2010 PubMedPubMedCentralCrossRefGoogle Scholar
  119. Wang J, Ben Hamida S, Darcq E et al (2012) Ethanol-mediated facilitation of AMPA receptor function in the dorsomedial striatum: implications for alcohol drinking behavior. J Neurosci 32(43):15124–15132. doi: 10.1523/JNEUROSCI.2783-12.2012 PubMedPubMedCentralCrossRefGoogle Scholar
  120. Wayner MJ, Greenberg I, Tartaglione R et al (1972) A new factor affecting the consumption of ethyl alcohol and other sapid fluids. Physiol Behav 8(2):345–362PubMedCrossRefGoogle Scholar
  121. Whitney G, Harder DB (1994) Genetics of bitter perception in mice. Physiol Behav 56(6):1141–1147PubMedCrossRefGoogle Scholar
  122. Wilcox MV, Cuzon Carlson VC, Sherazee N et al (2014) Repeated binge-like ethanol drinking alters ethanol drinking patterns and depresses striatal GABAergic transmission. Neuropsychopharmacology 39(3):579–594. doi: 10.1038/npp.2013.230 PubMedCrossRefGoogle Scholar
  123. Wise RA (1973) Voluntary ethanol intake in rats following exposure to ethanol on various schedules. Psychopharmacologia 29(3):203–210PubMedCrossRefGoogle Scholar
  124. Xie GQ, Wang SJ, Li J et al (2009) Ethanol attenuates the HFS-induced, ERK-mediated LTP in a dose-dependent manner in rat striatum. Alcohol Clin Exp Res 33(1):121–128. doi: 10.1111/j.1530-0277.2008.00818.x PubMedCrossRefGoogle Scholar
  125. Yaka R, Phamluong K, Ron D (2003) Scaffolding of Fyn kinase to the NMDA receptor determines brain region sensitivity to ethanol. J Neurosci 23(9):3623–3632PubMedPubMedCentralGoogle Scholar
  126. Yin HH, Knowlton BJ (2004) Contributions of striatal subregions to place and response learning. Learn Mem 11(4):459–463. doi: 10.1101/lm.81004 PubMedPubMedCentralCrossRefGoogle Scholar
  127. Yin HH, Knowlton BJ (2006) The role of the basal ganglia in habit formation. Nat Rev Neurosci 7(6):464–476. doi: 10.1038/nrn1919 PubMedCrossRefGoogle Scholar
  128. 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):181–189PubMedCrossRefGoogle Scholar
  129. Yin HH, Ostlund SB, Knowlton BJ et al (2005) The role of the dorsomedial striatum in instrumental conditioning. Eur J Neurosci 22(2):513–523. doi: 10.1111/j.1460-9568.2005.04218.x PubMedCrossRefGoogle Scholar
  130. Yin HH, Park BS, Adermark L, Lovinger DM (2007) Ethanol reverses the direction of long-term synaptic plasticity in the dorsomedial striatum. Eur J Neurosci 25(11):3226–3232. doi: 10.1111/j.1460-9568.2007.05606.x PubMedCrossRefGoogle Scholar
  131. Zhang TA, Hendricson AW, Morrisett RA (2005) Dual synaptic sites of D(1)-dopaminergic regulation of ethanol sensitivity of NMDA receptors in nucleus accumbens. Synapse 58(1):30–44. doi: 10.1002/syn.20181 PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Mary H. Patton
    • 1
  • Aparna P. Shah
    • 1
  • Brian N. Mathur
    • 1
    Email author
  1. 1.Department of PharmacologyUniversity of Maryland School of MedicineBaltimoreUSA

Personalised recommendations