Chronic alcohol disrupts dopamine receptor activity and the cognitive function of the medial prefrontal cortex

Journal of Neuroscience

Volumn 34, Issue 10, 2014, Pages 3706-3718

  Trantham Davidson, Heather ^a   Burnett, Elizabeth J ^a   Gass, Justin T ^a   Lopez, Marcelo F ^a   Mulholland, Patrick J ^a   Centanni, Samuel W ^a   Floresco, Stan B ^b   Judson Chandler, L ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Alcohol; Cognitive; D2 D4; Dopamine; mGluR1; PFC

Indexed keywords

DOPAMINE RECEPTOR; RECEPTOR SUBTYPE;

ADULT; ALCOHOL BLOOD LEVEL; ALCOHOL INTOXICATION; ALCOHOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASSOCIATION; AUTORADIOGRAPHY; BEHAVIOR DISORDER; COGNITION; CONTROLLED STUDY; ELECTROPHYSIOLOGICAL PROCEDURES; EXECUTIVE FUNCTION; EXPERIMENTAL BEHAVIORAL TEST; FRONTAL CORTEX; IMMUNOCHEMISTRY; INTERNEURON; INTRACELLULAR SIGNALING; MALE; NERVE POTENTIAL; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; VISUAL DISCRIMINATION; VOLTAGE CLAMP TECHNIQUE; WESTERN BLOTTING;

ALCOHOL; COGNITIVE; D2/D4; DOPAMINE; MGLUR1; PFC;

ANIMALS; COGNITION; CONDITIONING, OPERANT; ETHANOL; MALE; PHOTIC STIMULATION; PREFRONTAL CORTEX; PSYCHOMOTOR PERFORMANCE; RANDOM ALLOCATION; RATS; RATS, LONG-EVANS; RECEPTORS, DOPAMINE D2; RECEPTORS, DOPAMINE D4;

EID: 84895489827     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0623-13.2014     Document Type: Article

References (64)

1. Arnsten AF, Cai JX, Murphy BL, Goldman-Rakic PS (1994) Dopamine D1 receptor mechanisms in the cognitive performance of young adult and aged monkeys. Psychopharmacology 116:143-151. CrossRef Medline
2. Beazely MA, Tong A, Wei WL, Van Tol H, Sidhu B, MacDonald JF (2006) D2-class dopamine receptor inhibition of NMDA currents in prefrontal cortical neurons is platelet-derived growth factor receptor-dependent. J Neurochem 98:1657-1663. CrossRef Medline
3. Bergman H, Engelbrektson K, Fransson A, Herlitz K, Hindmarsh T, Neiman J (1998) [Alcohol-induced cognitive impairment is reversible. Neuropsychological tests but not MRT show improvement after abstinence]. Lakartidningen 95:4228, 4231-4236. Medline
4. Beveridge TJ, Smith HR, Nader MA, Porrino LJ (2009) Abstinence from chronic cocaine self-administration alters striatal dopamine systems in rhesus monkeys. Neuropsychopharmacology 34:1162-1171. CrossRef Medline
5. Bice PJ, Liang T, Zhang L, Strother WN, Carr LG (2008) Drd2 expression in the high alcohol-preferring and low alcohol-preferring mice. Mamm Genome 19:69-76. CrossRef Medline
6. Blume LC, Bass CE, Childers SR, Dalton GD, Roberts DC, Richardson JM, Xiao R, Selley DE, Howlett AC (2013) Striatal CB1 and D2 receptors regulate expression of each other, CRIP1A and delta opioid systems. J Neurochem 124:808-820. CrossRef Medline
7. Campanella S, Petit G, Maurage P, Kornreich C, Verbanck P, Noël X (2009) Chronic alcoholism: insights from neurophysiology. Neurophysiol Clin 39:191-207. CrossRef Medline
8. Campanella S, Petit G, Verbanck P, Kornreich C, Noel X (2011) How cognitive assessment through clinical neurophysiology may help optimize chronic alcoholism treatment. Neurophysiol Clin 41:115-123. CrossRef Medline
9. Charney DA, Zikos E, Gill KJ (2010) Early recovery from alcohol dependence: factors that promote or impede abstinence. J Subst Abuse Treat 38:42-50. CrossRef Medline
10. Chow A, Erisir A, Farb C, Nadal MS, Ozaita A, Lau D, Welker E, Rudy B (1999) K(+) channel expression distinguishes subpopulations of parvalbuminand somatostatin-containing neocortical interneurons. J Neurosci 19:9332-9345. Medline
11. Compte A, Brunel N, Goldman-Rakic PS, Wang XJ (2000) Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. Cereb Cortex 10:910-923. CrossRef Medline
12. Cools R, D'EspositoM (2011) Inverted-U-shaped dopamine actions on human working memory and cognitive control. Biol Psychiatry 69:e113-25. CrossRef Medline
13. Durstewitz D, Seamans JK, Sejnowski TJ (2000) Dopamine-mediated stabilization of delay-period activity in a network model of prefrontal cortex. J Neurophysiol 83:1733-1750. Medline
14. Erisir A, Lau D, Rudy B, Leonard CS (1999) Function of specific K(+) channels in sustained high-frequency firing of fast-spiking neocortical interneurons. J Neurophysiol 82:2476-2489. Medline
15. Finn PR, Justus A, Mazas C, Steinmetz JE (1999) Working memory, executive processes and the effects of alcohol on Go/No-Go learning: testing a model of behavioral regulation and impulsivity. Psychopharmacology 146:465-472. CrossRef Medline
16. Floresco SB, Magyar O (2006) Mesocortical dopamine modulation of executive functions: beyond working memory. Psychopharmacology 188: 567-585. CrossRef Medline
17. Floresco SB, Magyar O, Ghods-Sharifi S, Vexelman C, Tse MT (2006) Multiple dopamine receptor subtypes in the medial prefrontal cortex of the rat regulate set-shifting. Neuropsychopharmacology 31:297-309. CrossRef Medline
18. Floresco SB, Block AE, Tse MT (2008) Inactivation of the medial prefrontal cortex of the rat impairs strategy set-shifting, but not reversal learning, using a novel, automated procedure. Behav Brain Res 190:85-96. CrossRef Medline
19. Gan L, Falzone TL, Zhang K, Rubinstein M, Baldessarini RJ, Tarazi FI (2004) Enhanced expression of dopamine D(1) and glutamate NMDA receptors in dopamine D(4) receptor knockout mice. J Mol Neurosci 22:167-178. CrossRef Medline
20. Gao WJ, Goldman-Rakic PS (2003) Selective modulation of excitatory and inhibitory microcircuits by dopamine. Proc Natl Acad Sci U S A 100: 2836-2841. CrossRef Medline
21. Gao WJ, Wang Y, Goldman-Rakic PS (2003) Dopamine modulation of perisomatic and peridendritic inhibition in prefrontal cortex. J Neurosci 23:1622-1630. Medline
22. Garzón M, Duffy AM, Chan J, Lynch MK, Mackie K, Pickel VM (2013) Dopamine D(2) and acetylcholine alpha7 nicotinic receptors have subcellular distributions favoring mediation of convergent signaling in the mouse ventral tegmental area. Neuroscience 252:126-143. CrossRef Medline
23. Goldberg EM, Watanabe S, Chang SY, Joho RH, Huang ZJ, Leondard CS, Rudy B (2005) Specific functions of synaptically localized potassium channels in synaptic transmission at the neocortical GABAergic fastspiking cell synapse. J Neurosci 25:5230-5235. CrossRef Medline
24. Goldberg EM, Jeong HY, Kruglikov I, Tremblay R, Lazarenko RM, Rudy B (2011) Rapid developmental maturation of neocortical FS cell intrinsic excitability. Cereb Cortex 21:666-682. CrossRef Medline
25. Haluk DM, Floresco SB (2009) Ventral striatal dopamine modulation of different forms of behavioral flexibility. Neuropsychopharmacology 34: 2041-2052. CrossRef Medline
26. Harvey M, Lau D, Civillico E, Rudy B, Contreras D (2012) Impaired longrange synchronization of gamma oscillations in the neocortex of a mouse lacking Kv3.2 potassium channels. J Neurophysiol 108:827-833. CrossRef Medline
27. Holmes A, Fitzgerald PJ, MacPherson KP, DeBrouse L, Colacicco G, Flynn SM, Masneuf S, Pleil KE, Li C, Marcinkiewcz CA, Kash TL, Gunduz-Cinar O, Camp M (2012) Chronic alcohol remodels prefrontal neurons and disrupts NMDAR-mediated fear extinction encoding. Nat Neurosci 15: 1359-1361. CrossRef Medline
28. Hutchison KE, McGeary J, Smolen A, Bryan A, Swift RM (2002) The DRD4 VNTR polymorphism moderates craving after alcohol consumption. Health Psychol 21:139-146. CrossRef Medline
29. Kraschewski A, Reese J, Anghelescu I, Winterer G, Schmidt LG, Gallinat J, Finckh U, Rommelspacher H, Wernicke C (2009) Association of the dopamine D2 receptor gene with alcohol dependence: haplotypes and subgroups of alcoholics as key factors for understanding receptor function. Pharmacogenet Genomics 19:513-527. CrossRef Medline
30. Kroener S, Lavin A (2010) Altered dopamine modulation of inhibition in the prefrontal cortex of cocaine-sensitized rats. Neuropsychopharmacology 35:2292-2304. CrossRef Medline
31. Kroener S, Mulholland PJ, New NN, Gass JT, Becker HC, Chandler LJ (2012) Chronic alcohol exposure alters behavioral and synaptic plasticity of the rodent prefrontal cortex. PLoS One 7:e37541. CrossRef Medline
32. Lee B, London ED, Poldrack RA, Farahi J, Nacca A, Monterosso JR, Mumford JA, Bokarius AV, Dahlbom M, Mukherjee J, Bilder RM, Brody AL, Mandelkern MA (2009) Striatal dopamine d2/d3 receptor availability is reduced in methamphetamine dependence and is linked to impulsivity. J Neurosci 29:14734-14740. CrossRef Medline
33. Lewis DA, Sesack SR, Levey AI, Rosenberg DR (1998) Dopamine axons in primate prefrontal cortex: specificity of distribution, synaptic targets, and development. Adv Pharmacol 42:703-706. Medline
34. Moreno H, Kentros C, Bueno E, Weiser M, Hernandez A, Vega-Saenz de Miera E, Ponce A, Thornhill W, Rudy B (1995) Thalamocortical projections have a K+ channel that is phosphorylated and modulated by cAMPdependent protein kinase. J Neurosci 15:5486-5501. Medline
35. Morganstern I, Tejani-Butt S (2010) Differential patterns of alcohol consumption and dopamine-2 receptor binding in Wistar-Kyoto and Wistar rats. Neurochem Res 35:1708-1715. CrossRef Medline
36. Mulholland PJ, Becker HC, Woodward JJ, Chandler LJ (2011) Small conductance calcium-activated potassium type 2 channels regulate alcoholassociated plasticity of glutamatergic synapses. Biol Psychiatry 69:625-632. CrossRef Medline
37. Myrick H, Anton R, Voronin K, Wang W, Henderson S (2007) A doubleblind evaluation of gabapentin on alcohol effects and drinking in a clinical laboratory paradigm. Alcohol Clin Exp Res 31:221-227. CrossRef Medline
38. Nixon K, Crews FT (2002) Binge ethanol exposure decreases neurogenesis in adult rat hippocampus. J Neurochem 83:1087-1093. CrossRef Medline
39. Noble EP (2000) Addiction and its reward process through polymorphisms of the D2 dopamine receptor gene: a review. Eur Psychiatry 15:79-89. CrossRef Medline
40. O'Dell LE, Roberts AJ, Smith RT, Koob GF (2004) Enhanced alcohol selfadministration after intermittent versus continuous alcohol vapor exposure. Alcohol Clin Exp Res 28:1676-1682. CrossRef Medline
41. Paspalas CD, Goldman-Rakic PS (2005) Presynaptic D1 dopamine receptors in primate prefrontal cortex: target-specific expression in the glutamatergic synapse. J Neurosci 25:1260-1267. CrossRef Medline
42. Paxinos G, Watson P (2007) The rat brain in stereotaxic coordinates, 6th edition. San Diego: Elsevier.
43. Prencipe L, Iaccheri E, Manzati C (1987) Enzymic ethanol assay: a new colorimetric method based on measurement of hydrogen peroxide. Clin Chem 33:486-489. Medline
44. Puig MV, Ushimaru M, Kawaguchi Y (2008) Two distinct activity patterns of fast-spiking interneurons during neocortical UP states. Proc Natl Acad Sci U S A 105:8428-8433. CrossRef Medline
45. Rando K, Hong KI, Bhagwagar Z, Li CS, Bergquist K, Guarnaccia J, Sinha R (2011) Association of frontal and posterior cortical gray matter volume with time to alcohol relapse: a prospective study. Am J Psychiatry 168: 183-192. CrossRef Medline
46. Rao SG, Williams GV, Goldman-Rakic PS (1999) Isodirectional tuning of adjacent interneurons and pyramidal cells during working memory: evidence for microcolumnar organization in PFC. J Neurophysiol 81:1903-1916. Medline
47. Richardson NR, Roberts DC (1996) Progressive ratio schedules in drug selfadministration studies in rats: a method to evaluate reinforcing efficacy. J Neurosci Methods 66:1-11. CrossRef Medline
48. Rudy B, Chow A, Lau D, Amarillo Y, Ozaita A, Saganich M, Moreno H, Nadal MS, Hernandez-Pineda R, Hernandez-Cruz A, Erisir A, Leonard C, Vega-Saenz de Miera E (1999) Contributions of Kv3 channels to neuronal excitability. Ann N Y Acad Sci 868:304-343. CrossRef Medline
49. Sabia S, Guéguen A, Berr C, Berkman L, Ankri J, Goldberg M, Zins M, Singh-Manoux A (2011) High alcohol consumption in middle-aged adults is associated with poorer cognitive performance only in the low socioeconomic group. Results from the GAZEL cohort study. Addiction 106: 93-101. CrossRef Medline
50. Schacht JP, Randall PK, Waid LR, Baros AM, Latham PK, Wright TM, Myrick H, Anton RF. (2011) Neurocognitive performance, alcohol withdrawal, and effects of a combination of flumazenil and gabapentin in alcohol dependence. Alcohol Clin Exp Res 35:2030-2038. CrossRef Medline
51. Sim LJ, Selley DE, Childers SR (1995) In vitro autoradiography of receptoractivated G proteins in rat brain by agonist-stimulated guanylyl 5-[gamma-[35S]thio]-triphosphate binding. Proc Natl Acad Sci U S A 92: 7242-7246. CrossRef Medline
52. Sullivan EV, Rosenbloom MJ, Pfefferbaum A (2000) Pattern of motor and cognitive deficits in detoxified alcoholic men. Alcohol Clin Exp Res 24: 611-621. CrossRef Medline
53. Sun H, Neugebauer V (2011) mGluR1, but not mGluR5, activates feedforward inhibition in the medial prefrontal cortex to impair decision making. J Neurophysiol 106:960-973. CrossRef Medline
54. Tedstone D, Coyle K (2004) Cognitive impairments in sober alcoholics: performance on selective and divided attention tasks. Drug Alcohol Depend 75:277-286. CrossRef Medline
55. Trantham-Davidson H, Kröner S, Seamans JK (2008) Dopamine modulation of prefrontal cortex interneurons occurs independently of DARPP-32. Cereb Cortex 18:951-958. CrossRef Medline
56. Tseng KY, O'Donnell P (2007) Dopamine modulation of prefrontal cortical interneurons changes during adolescence. Cereb Cortex 17:1235-1240. Medline
57. van der Zwaluw CS, Kuntsche E, Engels RC (2011) Risky alcohol use in adolescence: the role of genetics (DRD2, SLC6A4) and coping motives. Alcohol Clin Exp Res 35:756-764. CrossRef Medline
58. Volkow ND, Wang GJ, Fowler JS, Logan J, Hitzemann R, Ding YS, Pappas N, Shea C, Piscani K (1996) Decreases in dopamine receptors but not in dopamine transporters in alcoholics. Alcohol Clin Exp Res 20:1594-1598. CrossRef Medline
59. Volkow ND, Wang GJ, Maynard L, Fowler JS, Jayne B, Telang F, Logan J, Ding YS, Gatley SJ, Hitzemann R, Wong C, PappasN (2002) Effects of alcohol detoxification on dopamine D2 receptors in alcoholics: a preliminary study. Psychiatry Res 116:163-172. CrossRef Medline
60. Volkow ND, Wang GJ, Begleiter H, Porjesz B, Fowler JS, Telang F, Wong C, Ma Y, Logan J, Goldstein R, Alexoff D, Thanos PK (2006) High levels of dopamine D2 receptors in unaffected members of alcoholic families: possible protective factors. Arch Gen Psychiatry 63:999-1008. CrossRef Medline
61. Wang X, Zhong P, Gu Z, Yan Z (2003) Regulation of NMDA receptors by dopamine D4 signaling in prefrontal cortex. J Neurosci 23:9852-9861. Medline
62. Wicks S, Hammar J, Heilig M, Wisén O (2001) Factors affecting the shortterm prognosis of alcohol dependent patients undergoing inpatient detoxification. Subst Abus 22:235-245. CrossRef Medline
63. Wölwer W, Burtscheidt W, Redner C, Schwarz R, Gaebel W (2001) Outpatient behaviour therapy in alcoholism: impact of personality disorders and cognitive impairments. Acta Psychiatr Scand 103:30-37. CrossRef Medline
64. Zhang K, Grady CJ, Tsapakis EM, Andersen SL, Tarazi FI, Baldessarini RJ (2004) Regulation of working memory by dopamine D4 receptor in rats. Neuropsychopharmacology 29:1648-1655. CrossRef Medline