, Volume 231, Issue 12, pp 2493–2506 | Cite as

Alpha-synuclein deletion decreases motor impulsivity but does not affect risky decision making in a mouse Gambling Task

  • Yolanda Peña-Oliver
  • Sandra Sanchez-Roige
  • David N. Stephens
  • Tamzin L. Ripley
Original Investigation



There is evidence to support the role of alpha-synuclein in motor impulsivity, but the extrapolation of this finding to other types of impulsivity remains to be elucidated.


This study aims to investigate the role of alpha-synuclein in choice impulsivity/risky decision-making by means of a mouse version of the Iowa Gambling Task (mIGT).


Two strains of mice that differ in the expression of the alpha-synuclein gene, the C57BL/6JOlaHsd (HA) and C57BL/6J (CR), were tested in the mIGT. HA mice differ from their CR ancestors in possessing a chromosomal deletion resulting in the loss of two genes: snca, encoding alpha-synuclein and mmrn1, encoding multimerin-1. Mice were trained in the mIGT until a stable pattern of responding was achieved and then the acute effects of ethanol and cocaine in choice preference were investigated.


No differences between the strains were evident in risky decision-making in any of the experiments, but HA mice showed consistently reduced levels of premature responding in comparison with CR mice, confirming the reduced motor impulsivity found in a previous study. Ethanol did not modify the percentage of advantageous choices in either strain, while cocaine increased the risky choice behaviour by increasing the percentage of disadvantageous choices in both strains.


We provide further evidence for the involvement of alpha-synuclein in motor impulsivity and suggest that alpha-synuclein does not play a role in risky decision-making as evaluated in the mIGT.


Impulsivity Alpha-synuclein Iowa Gambling Task Mice Ethanol Cocaine 


  1. Abeliovich A, Schmitz Y, Farinas I, Choi-Lundberg D, Ho WH, Castillo PE, Shinsky N, Verdugo JM, Armanini M, Ryan A, Hynes M, Phillips H, Sulzer D, Rosenthal A (2000) Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 25:239–252PubMedCrossRefGoogle Scholar
  2. Adida M, Clark L, Pomietto P, Kaladjian A, Besnier N, Azorin JM, Jeanningros R, Goodwin GM (2008) Lack of insight may predict impaired decision making in manic patients. Bipolar Disord 10:829–837PubMedCrossRefGoogle Scholar
  3. Anwar S, Peters O, Millership S, Ninkina N, Doig N, Connor-Robson N, Threlfell S, Kooner G, Deacon RM, Bannerman DM, Bolam JP, Chandra SS, Cragg SJ, Wade-Martins R, Buchman VL (2011) Functional alterations to the nigrostriatal system in mice lacking all three members of the synuclein family. J Neurosci: Off J Soc Neurosci 31:7264–7274CrossRefGoogle Scholar
  4. Baarendse PJ, Vanderschuren LJ (2012) Dissociable effects of monoamine reuptake inhibitors on distinct forms of impulsive behavior in rats. Psychopharmacology 219:313–326PubMedCentralPubMedCrossRefGoogle Scholar
  5. Baarendse PJ, Winstanley CA, Vanderschuren LJ (2013) Simultaneous blockade of dopamine and noradrenaline reuptake promotes disadvantageous decision making in a rat gambling task. Psychopharmacology (Berl) 225:719–731CrossRefGoogle Scholar
  6. Bari A, Robbins TW (2013) Inhibition and impulsivity: behavioral and neural basis of response control. Prog Neurobiol 108:44–79PubMedCrossRefGoogle Scholar
  7. Bechara A, Damasio AR, Damasio H, Anderson SW (1994) Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50:7–15PubMedCrossRefGoogle Scholar
  8. Bechara A, Damasio H, Damasio AR, Lee GP (1999) Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making. J Neurosci 19:5473–5481PubMedGoogle Scholar
  9. Bechara A, Dolan S, Denburg N, Hindes A, Anderson SW, Nathan PE (2001) Decision-making deficits, linked to a dysfunctional ventromedial prefrontal cortex, revealed in alcohol and stimulant abusers. Neuropsychologia 39:376–389PubMedCrossRefGoogle Scholar
  10. Bezdjian S, Baker LA, Tuvblad C (2011) Genetic and environmental influences on impulsivity: a meta-analysis of twin, family and adoption studies. Clin Psychol Rev 31:1209–1223PubMedCentralPubMedCrossRefGoogle Scholar
  11. Bickel WK, Marsch LA (2001) Toward a behavioral economic understanding of drug dependence: delay discounting processes. Addiction 96:73–86PubMedCrossRefGoogle Scholar
  12. Bizarro L, Patel S, Stolerman IP (2003) Comprehensive deficits in performance of an attentional task produced by co-administering alcohol and nicotine to rats. Drug Alcohol Depend 72:287–295PubMedCrossRefGoogle Scholar
  13. Bonsch D, Reulbach U, Bayerlein K, Hillemacher T, Kornhuber J, Bleich S (2004) Elevated alpha synuclein mRNA levels are associated with craving in patients with alcoholism. Biol Psychiatry 56:984–986PubMedCrossRefGoogle Scholar
  14. Bonsch D, Greifenberg V, Bayerlein K, Biermann T, Reulbach U, Hillemacher T, Kornhuber J, Bleich S (2005) Alpha-synuclein protein levels are increased in alcoholic patients and are linked to craving. Alcohol Clin Exp Res 29:763–765PubMedCrossRefGoogle Scholar
  15. Brenz Verca MS, Bahi A, Boyer F, Wagner GC, Dreyer JL (2003) Distribution of alpha- and gamma-synucleins in the adult rat brain and their modification by high-dose cocaine treatment. Eur J Neurosci 18:1923–1938PubMedCrossRefGoogle Scholar
  16. Brevers D, Cleeremans A, Verbruggen F, Bechara A, Kornreich C, Verbanck P, Noel X (2012) Impulsive action but not impulsive choice determines problem gambling severity. PLoS One 7:e50647PubMedCentralPubMedCrossRefGoogle Scholar
  17. Brewer JA, Potenza MN (2008) The neurobiology and genetics of impulse control disorders: relationships to drug addictions. Biochem Pharmacol 75:63–75PubMedCentralPubMedCrossRefGoogle Scholar
  18. Broos N, Schmaal L, Wiskerke J, Kostelijk L, Lam T, Stoop N, Weierink L, Ham J, de Geus EJ, Schoffelmeer AN, van den Brink W, Veltman DJ, de Vries TJ, Pattij T, Goudriaan AE (2012) The relationship between impulsive choice and impulsive action: a cross-species translational study. PLoS One 7:e36781PubMedCentralPubMedCrossRefGoogle Scholar
  19. Cantrell H, Finn PR, Rickert ME, Lucas J (2008) Decision making in alcohol dependence: insensitivity to future consequences and comorbid disinhibitory psychopathology. Alcohol Clin Exp Res 32:1398–1407PubMedCentralPubMedCrossRefGoogle Scholar
  20. Cavedini P, Riboldi G, Keller R, D'Annucci A, Bellodi L (2002) Frontal lobe dysfunction in pathological gambling patients. Biol Psychiatry 51:334–341PubMedCrossRefGoogle Scholar
  21. Chartier-Harlin MC, Kachergus J, Roumier C, Mouroux V, Douay X, Lincoln S, Levecque C, Larvor L, Andrieux J, Hulihan M, Waucquier N, Defebvre L, Amouyel P, Farrer M, Destee A (2004) Alpha-synuclein locus duplication as a cause of familial Parkinson's disease. Lancet 364:1167–1169PubMedCrossRefGoogle Scholar
  22. Cherpitel CJ (1999) Substance use, injury, and risk-taking dispositions in the general population. Alcohol Clin Exp Res 23:121–126PubMedCrossRefGoogle Scholar
  23. Dagher A, Robbins TW (2009) Personality, addiction, dopamine: insights from Parkinson's disease. Neuron 61:502–510PubMedCrossRefGoogle Scholar
  24. Dalley JW, Everitt BJ, Robbins TW (2011) Impulsivity, compulsivity, and top-down cognitive control. Neuron 69:680–694PubMedCrossRefGoogle Scholar
  25. de Visser L, Homberg JR, Mitsogiannis M, Zeeb FD, Rivalan M, Fitoussi A, Galhardo V, van den Bos R, Winstanley CA, Dellu-Hagedorn F (2011) Rodent versions of the Iowa gambling task: opportunities and challenges for the understanding of decision-making. Front Neurosci 5:109PubMedCentralPubMedGoogle Scholar
  26. Diergaarde L, Pattij T, Poortvliet I, Hogenboom F, de Vries W, Schoffelmeer AN, De Vries TJ (2008) Impulsive choice and impulsive action predict vulnerability to distinct stages of nicotine seeking in rats. Biol Psychiatry 63:301–308PubMedCrossRefGoogle Scholar
  27. Dougherty DM, Marsh-Richard DM, Hatzis ES, Nouvion SO, Mathias CW (2008) A test of alcohol dose effects on multiple behavioral measures of impulsivity. Drug Alcohol Depend 96:111–120PubMedCentralPubMedCrossRefGoogle Scholar
  28. Ericksen KP, Trocki KF (1994) Sex, alcohol and sexually transmitted diseases: a national survey. Fam Plan Perspect 26:257–263CrossRefGoogle Scholar
  29. Evenden JL (1999) Varieties of impulsivity. Psychopharmacology (Berl) 146:348–361CrossRefGoogle Scholar
  30. Evenden JL, Ryan CN (1999) The pharmacology of impulsive behaviour in rats VI: the effects of ethanol and selective serotonergic drugs on response choice with varying delays of reinforcement. Psychopharmacology (Berl) 146:413–421CrossRefGoogle Scholar
  31. Fellows LK, Farah MJ (2005) Different underlying impairments in decision-making following ventromedial and dorsolateral frontal lobe damage in humans. Cereb Cortex 15:58–63PubMedCrossRefGoogle Scholar
  32. Fineberg NA, Potenza MN, Chamberlain SR, Berlin HA, Menzies L, Bechara A, Sahakian BJ, Robbins TW, Bullmore ET, Hollander E (2010) Probing compulsive and impulsive behaviors, from animal models to endophenotypes: a narrative review. Neuropsychopharmacology 35:591–604PubMedCentralPubMedCrossRefGoogle Scholar
  33. Fletcher PJ, Rizos Z, Noble K, Higgins GA (2011) Impulsive action induced by amphetamine, cocaine and MK801 is reduced by 5-HT(2C) receptor stimulation and 5-HT(2A) receptor blockade. Neuropharmacology 61:468–477PubMedCrossRefGoogle Scholar
  34. Fletcher PJ, Soko AD, Higgins GA (2012) Impulsive action in the 5-choice serial reaction time test in 5-HT2C receptor null mutant mice. Psychopharmacology (Berl) 226:561–570CrossRefGoogle Scholar
  35. Fornai F, Lenzi P, Ferrucci M, Lazzeri G, di Poggio AB, Natale G, Busceti CL, Biagioni F, Giusiani M, Ruggieri S, Paparelli A (2005) Occurrence of neuronal inclusions combined with increased nigral expression of alpha-synuclein within dopaminergic neurons following treatment with amphetamine derivatives in mice. Brain Res Bull 65:405–413PubMedCrossRefGoogle Scholar
  36. Foroud T, Wetherill LF, Liang T, Dick DM, Hesselbrock V, Kramer J, Nurnberger J, Schuckit M, Carr L, Porjesz B, Xuei X, Edenberg HJ (2007) Association of alcohol craving with alpha-synuclein (SNCA). Alcohol Clin Exp Res 31:537–545PubMedCrossRefGoogle Scholar
  37. George S, Rogers RD, Duka T (2005) The acute effect of alcohol on decision making in social drinkers. Psychopharmacology (Berl) 182:160–169CrossRefGoogle Scholar
  38. Hellemans KG, Nobrega JN, Olmstead MC (2005) Early environmental experience alters baseline and ethanol-induced cognitive impulsivity: relationship to forebrain 5-HT1A receptor binding. Behav Brain Res 159:207–220PubMedCrossRefGoogle Scholar
  39. Homberg JR, van den Bos R, den Heijer E, Suer R, Cuppen E (2008) Serotonin transporter dosage modulates long-term decision-making in rat and human. Neuropharmacology 55:80–84PubMedCrossRefGoogle Scholar
  40. Izquierdo A, Jentsch JD (2012) Reversal learning as a measure of impulsive and compulsive behavior in addictions. Psychopharmacology (Berl) 219:607–620CrossRefGoogle Scholar
  41. Kjome KL, Lane SD, Schmitz JM, Green C, Ma L, Prasla I, Swann AC, Moeller FG (2010) Relationship between impulsivity and decision making in cocaine dependence. Psychiatry Res 178:299–304PubMedCentralPubMedCrossRefGoogle Scholar
  42. Lane SD, Cherek DR, Pietras CJ, Tcheremissine OV (2004) Alcohol effects on human risk taking. Psychopharmacology (Berl) 172:68–77CrossRefGoogle Scholar
  43. Le Berre AP, Rauchs G, La Joie R, Mezenge F, Boudehent C, Vabret F, Segobin S, Viader F, Allain P, Eustache F, Pitel AL, Beaunieux H (2012) Impaired decision-making and brain shrinkage in alcoholism. Eur Psychiatry. doi:10.1016/j.eurpsy.2012.10.002 PubMedGoogle Scholar
  44. Lewohl JM, Huygens F, Crane DI, Dodd PR (2001) GABA(A) receptor alpha-subunit proteins in human chronic alcoholics. J Neurochem 78:424–434PubMedCrossRefGoogle Scholar
  45. Loeber S, Duka T, Welzel H, Nakovics H, Heinz A, Flor H, Mann K (2009) Impairment of cognitive abilities and decision making after chronic use of alcohol: the impact of multiple detoxifications. Alcohol Alcohol 44:372–381PubMedCrossRefGoogle Scholar
  46. Loeber S, Duka T, Welzel Marquez H, Nakovics H, Heinz A, Mann K, Flor H (2010) Effects of repeated withdrawal from alcohol on recovery of cognitive impairment under abstinence and rate of relapse. Alcohol Alcohol 45:541–547PubMedCrossRefGoogle Scholar
  47. Mash DC, Ouyang Q, Pablo J, Basile M, Izenwasser S, Lieberman A, Perrin RJ (2003) Cocaine abusers have an overexpression of alpha-synuclein in dopamine neurons. The Journal of Neuroscience: the official journal of the Society for Neuroscience 23:2564–2571Google Scholar
  48. Mazas CA, Finn PR, Steinmetz JE (2000) Decision-making biases, antisocial personality, and early-onset alcoholism. Alcohol Clin Exp Res 24:1036–1040PubMedCrossRefGoogle Scholar
  49. Miranda R Jr, MacKillop J, Meyerson LA, Justus A, Lovallo WR (2009) Influence of antisocial and psychopathic traits on decision-making biases in alcoholics. Alcohol Clin Exp Res 33:817–825PubMedCentralPubMedCrossRefGoogle Scholar
  50. Mitchell MR, Vokes CM, Blankenship AL, Simon NW, Setlow B (2011) Effects of acute administration of nicotine, amphetamine, diazepam, morphine, and ethanol on risky decision-making in rats. Psychopharmacology (Berl) 218:703–712CrossRefGoogle Scholar
  51. Murphy DD, Rueter SM, Trojanowski JQ, Lee VM (2000) Synucleins are developmentally expressed, and alpha-synuclein regulates the size of the presynaptic vesicular pool in primary hippocampal neurons. J Neurosci: Off J Soc Neurosci 20:3214–3220Google Scholar
  52. Nemani VM, Lu W, Berge V, Nakamura K, Onoa B, Lee MK, Chaudhry FA, Nicoll RA, Edwards RH (2010) Increased expression of alpha-synuclein reduces neurotransmitter release by inhibiting synaptic vesicle reclustering after endocytosis. Neuron 65:66–79PubMedCentralPubMedCrossRefGoogle Scholar
  53. Oliver YP, Ripley TL, Stephens DN (2009) Ethanol effects on impulsivity in two mouse strains: similarities to diazepam and ketamine. Psychopharmacology (Berl) 204:679–692CrossRefGoogle Scholar
  54. Olmstead MC, Hellemans KG, Paine TA (2006) Alcohol-induced impulsivity in rats: an effect of cue salience? Psychopharmacology (Berl) 184:221–228CrossRefGoogle Scholar
  55. Ortner CN, MacDonald TK, Olmstead MC (2003) Alcohol intoxication reduces impulsivity in the delay-discounting paradigm. Alcohol Alcohol 38:151–156PubMedCrossRefGoogle Scholar
  56. Pattij T, Vanderschuren LJ (2008) The neuropharmacology of impulsive behaviour. Trends Pharmacol Sci 29:192–199PubMedCrossRefGoogle Scholar
  57. Pena-Oliver Y, Buchman VL, Dalley JW, Robbins TW, Schumann G, Ripley TL, King SL, Stephens DN (2012) Deletion of alpha-synuclein decreases impulsivity in mice. Genes Brain Behav 11:137–146PubMedCentralPubMedCrossRefGoogle Scholar
  58. Poulos CX, Parker JL, Le DA (1998) Increased impulsivity after injected alcohol predicts later alcohol consumption in rats: evidence for "loss-of-control drinking" and marked individual differences. Behav Neurosci 112:1247–1257PubMedCrossRefGoogle Scholar
  59. Qin Y, Ouyang Q, Pablo J, Mash DC (2005) Cocaine abuse elevates alpha-synuclein and dopamine transporter levels in the human striatum. Neuroreport 16:1489–1493PubMedCrossRefGoogle Scholar
  60. Ramaekers JG, Kuypers KP (2006) Acute effects of 3,4-methylenedioxymethamphetamine (MDMA) on behavioral measures of impulsivity: alone and in combination with alcohol. Neuropsychopharmacology 31:1048–1055PubMedCrossRefGoogle Scholar
  61. Reynolds B, Richards JB, de Wit H (2006) Acute-alcohol effects on the Experiential Discounting Task (EDT) and a question-based measure of delay discounting. Pharmacol Biochem Behav 83:194–202PubMedCrossRefGoogle Scholar
  62. Richards JB, Zhang L, Mitchell SH, de Wit H (1999) Delay or probability discounting in a model of impulsive behavior: effect of alcohol. J Exp Anal Behav 71:121–143PubMedCentralPubMedCrossRefGoogle Scholar
  63. Ridderinkhof KR, de Vlugt Y, Bramlage A, Spaan M, Elton M, Snel J, Band GP (2002) Alcohol consumption impairs detection of performance errors in mediofrontal cortex. Science 298:2209–2211PubMedCrossRefGoogle Scholar
  64. Rivalan M, Ahmed SH, Dellu-Hagedorn F (2009) Risk-prone individuals prefer the wrong options on a rat version of the Iowa Gambling Task. Biol Psychiatry 66:743–749PubMedCrossRefGoogle Scholar
  65. Salgado JV, Malloy-Diniz LF, Campos VR, Abrantes SS, Fuentes D, Bechara A, Correa H (2009) Neuropsychological assessment of impulsive behavior in abstinent alcohol-dependent subjects. Rev Bras Psiquiatr 31:4–9PubMedCrossRefGoogle Scholar
  66. Sanchez-Roige S, Pena-Oliver Y, Stephens DN (2012) Measuring impulsivity in mice: the five-choice serial reaction time task. Psychopharmacology 219:253–270PubMedCrossRefGoogle Scholar
  67. Semenova S (2012) Attention, impulsivity, and cognitive flexibility in adult male rats exposed to ethanol binge during adolescence as measured in the five-choice serial reaction time task: the effects of task and ethanol challenges. Psychopharmacology (Berl) 219:433–442CrossRefGoogle Scholar
  68. Senior SL, Ninkina N, Deacon R, Bannerman D, Buchman VL, Cragg SJ, Wade-Martins R (2008) Increased striatal dopamine release and hyperdopaminergic-like behaviour in mice lacking both alpha-synuclein and gamma-synuclein. Eur J Neurosci 27:947–957PubMedCentralPubMedCrossRefGoogle Scholar
  69. Simon NW, Mendez IA, Setlow B (2007) Cocaine exposure causes long-term increases in impulsive choice. Behav Neurosci 121:543–549PubMedCentralPubMedCrossRefGoogle Scholar
  70. Singleton AB, Farrer M, Johnson J, Singleton A, Hague S, Kachergus J, Hulihan M, Peuralinna T, Dutra A, Nussbaum R, Lincoln S, Crawley A, Hanson M, Maraganore D, Adler C, Cookson MR, Muenter M, Baptista M, Miller D, Blancato J, Hardy J, Gwinn-Hardy K (2003) alpha-Synuclein locus triplication causes Parkinson's disease. Science 302:841PubMedCrossRefGoogle Scholar
  71. Solanto MV, Abikoff H, Sonuga-Barke E, Schachar R, Logan GD, Wigal T, Hechtman L, Hinshaw S, Turkel E (2001) The ecological validity of delay aversion and response inhibition as measures of impulsivity in AD/HD: a supplement to the NIMH multimodal treatment study of AD/HD. J Abnorm Child Psychol 29:215–228PubMedCrossRefGoogle Scholar
  72. Specht CG, Schoepfer R (2001) Deletion of the alpha-synuclein locus in a subpopulation of C57BL/6 J inbred mice. BMC Neurosci 2:11PubMedCentralPubMedCrossRefGoogle Scholar
  73. Specht CG, Schoepfer R (2004) Deletion of multimerin-1 in alpha-synuclein-deficient mice. Genomics 83:1176–1178PubMedCrossRefGoogle Scholar
  74. Steele CM, Southwick L (1985) Alcohol and social behavior I: the psychology of drunken excess. J Pers Soc Psychol 48:18–34PubMedCrossRefGoogle Scholar
  75. Tchanturia K, Liao PC, Uher R, Lawrence N, Treasure J, Campbell IC (2007) An investigation of decision making in anorexia nervosa using the Iowa Gambling Task and skin conductance measurements. J Int Neuropsychol Soc 13:635–641PubMedGoogle Scholar
  76. Tomie A, Aguado AS, Pohorecky LA, Benjamin D (1998) Ethanol induces impulsive-like responding in a delay-of-reward operant choice procedure: impulsivity predicts autoshaping. Psychopharmacology (Berl) 139:376–382CrossRefGoogle Scholar
  77. Urcelay GP, Dalley JW (2011) Linking ADHD, impulsivity, and drug abuse: a neuropsychological perspective. Curr Top Behav Neurosci. doi:10.1007/7854_2011_119 Google Scholar
  78. van den Bos R, Lasthuis W, den Heijer E, van der Harst J, Spruijt B (2006) Toward a rodent model of the Iowa gambling task. Behav Res Methods 38:470–478PubMedCrossRefGoogle Scholar
  79. van Enkhuizen J, Geyer MA, Young JW (2013) Differential effects of dopamine transporter inhibitors in the rodent Iowa gambling task: relevance to mania. Psychopharmacology 225:661–674PubMedCentralPubMedCrossRefGoogle Scholar
  80. van Gaalen MM, Brueggeman RJ, Bronius PF, Schoffelmeer AN, Vanderschuren LJ (2006a) Behavioral disinhibition requires dopamine receptor activation. Psychopharmacology 187:73–85PubMedCrossRefGoogle Scholar
  81. van Gaalen MM, van Koten R, Schoffelmeer AN, Vanderschuren LJ (2006b) Critical involvement of dopaminergic neurotransmission in impulsive decision making. Biol Psychiatry 60:66–73PubMedCrossRefGoogle Scholar
  82. Verdejo-Garcia AJ, Perales JC, Perez-Garcia M (2007) Cognitive impulsivity in cocaine and heroin polysubstance abusers. Addict Behav 32:950–966PubMedCrossRefGoogle Scholar
  83. Walker SE, Pena-Oliver Y, Stephens DN (2011) Learning not to be impulsive: disruption by experience of alcohol withdrawal. Psychopharmacology (Berl) 217:433–442CrossRefGoogle Scholar
  84. Wilhelm CJ, Mitchell SH (2012) Acute ethanol does not always affect delay discounting in rats selected to prefer or avoid ethanol. Alcohol Alcohol 47:518–524PubMedCentralPubMedCrossRefGoogle Scholar
  85. Winstanley CA (2011) The utility of rat models of impulsivity in developing pharmacotherapies for impulse control disorders. Br J Pharmacol 164:1301–1321PubMedCentralPubMedCrossRefGoogle Scholar
  86. Winstanley CA, Eagle DM, Robbins TW (2006) Behavioral models of impulsivity in relation to ADHD: translation between clinical and preclinical studies. Clin Psychol Rev 26:379–395PubMedCentralPubMedCrossRefGoogle Scholar
  87. Zeeb FD, Robbins TW, Winstanley CA (2009) Serotonergic and dopaminergic modulation of gambling behavior as assessed using a novel rat gambling task. Neuropsychopharmacology 34:2329–2343PubMedCrossRefGoogle Scholar
  88. Zeeb FD, Wong AC, Winstanley CA (2013) Differential effects of environmental enrichment, social-housing, and isolation-rearing on a rat gambling task: dissociations between impulsive action and risky decision-making. Psychopharmacology 225:381–395PubMedCrossRefGoogle Scholar
  89. Zou F, Chai HS, Younkin CS, Allen M, Crook J, Pankratz VS, Carrasquillo MM, Rowley CN, Nair AA, Middha S, Maharjan S, Nguyen T, Ma L, Malphrus KG, Palusak R, Lincoln S, Bisceglio G, Georgescu C, Kouri N, Kolbert CP, Jen J, Haines JL, Mayeux R, Pericak-Vance MA, Farrer LA, Schellenberg GD, Petersen RC, Graff-Radford NR, Dickson DW, Younkin SG, Ertekin-Taner N (2012) Brain expression genome-wide association study (eGWAS) identifies human disease-associated variants. PLoS Genet 8:e1002707PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Yolanda Peña-Oliver
    • 1
    • 2
  • Sandra Sanchez-Roige
    • 1
  • David N. Stephens
    • 1
  • Tamzin L. Ripley
    • 1
  1. 1.School of PsychologyUniversity of SussexBrightonUK
  2. 2.Department of PsychologyUniversity of CambridgeCambridgeUK

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