The moderating role of the dopamine transporter 1 gene on P50 sensory gating and its modulation by nicotine

Neuroscience

Volumn 180, Issue , 2011, Pages 148-156

  Millar, A ^a   Smith, D ^a,b   Choueiry, J ^b   Fisher, D ^c   Albert, P ^a   Knott, V ^a,b,c  

^a UNIVERSITY OF OTTAWA   (Canada)

^b ROYAL OTTAWA HOSPITAL   (Canada)

^c CARLETON UNIVERSITY   (Canada)

Author keywords

Dopamine transporter gene; Gating; Nicotine; P50; Schizophrenia; Smoking

Indexed keywords

DOPAMINE TRANSPORTER; NICOTINE GUM; PLACEBO;

ADULT; ALLELE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; CROSSOVER PROCEDURE; DOUBLE BLIND PROCEDURE; EVOKED AUDITORY RESPONSE; GENE EXPRESSION; HETEROZYGOTE; HUMAN; HUMAN EXPERIMENT; LATENT PERIOD; MALE; NEUROMODULATION; NORMAL HUMAN; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; SENSORY GATING; SMOKING;

ADOLESCENT; ADULT; BRAIN; CROSS-OVER STUDIES; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; DOUBLE-BLIND METHOD; EVOKED POTENTIALS, AUDITORY; FEMALE; GENOTYPE; HUMANS; MALE; NICOTINE; NICOTINIC AGONISTS; POLYMERASE CHAIN REACTION; SCHIZOPHRENIA; SENSORY GATING; YOUNG ADULT;

EID: 79953205899     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.02.008     Document Type: Article

References (89)

1. Adler L., Hoffer L., Griffith J., Waldo M., Freedman R. Normalization by nicotine of deficient auditory sensory gating in the relatives of schizophrenics. Biol Psychiatry 1992, 32:607-616.
2. Adler L., Hoffer B., Wiser A., Freedman R. Normalization of auditory physiology by cigarette smoking in schizophrenic patients. Am J Psychiatry 1993, 150:1856-1861.
3. Adler L., Olincy A., Cawthra E., McRae K., Harris J., Nagamoto H., Waldo M., Hall M., Bowles A., Woodward L., Ross R., Freedman R. Varied effects of atypical neuroleptics on P50 auditory gating in schizophrenia patients. Am J Psychiatry 2004, 161:1022-1028.
4. Adler L., Rose G., Freedman R. Neurophysiological studies of sensory gating in rats: effects of amphetamine, phencyclidine, and haloperidol. Biol Psychiatry 1986, 21:787-798.
5. Allen N., Bagade S., McQueen M., Ioannidis J., Kowoura F., Khoury M., Tanzi R., Bertram L. Systematic meta-analyses and field synapsis of genetic association studies in schizophrenia. The SzGene database. Nat Genet 2008, 40:827-834.
6. Baker M., Adler L., Franks R., Waldo M., Berry S., Nagamoto H., Muckle A., Freedman R. Neurophysiological assessment of sensory gating in psychiatric inpatients. Comparison between schizophrenia and other diagnoses. Biol Psychiatry 1987, 22:603-617.
7. Bertolino A., Blasi C., Latorre V., Rubino V., Rampino A., Sinibaldi L., Caforio G., Petruzella V., Pizzuti A., Scarabino A., Nardini M., Weinberger D., Dallapiccola B. Additive effects of genetic variation in dopamine regulating genes on working memory cortical activity in human brain. J Neurosci 2006, 261:3918-3922.
8. Boutros N., Korgyukov O., Jansen B., Feingold A., Bell M. Sensory gating deficits during the mid-latency phase of information processing in medicated schizophrenia patients. Psychiatry Res 2004, 126:203-215.
9. Bramon E., Rabe-Hesketh S., Sham P., Murray R., Frangov S. Meta-analysis of the P300 and P50 waveforms in schizophrenia. Schizophr Res 2004, 70:315-329.
10. Brenner C., Kieffaber P., Clementz B., Johannesen J., Shekhar A., O'Donnell B., Hetrick W. Event-related potential abnormalities in schizophrenia: a failure to "gate in" salient information?. Schizophr Res 2009, 113:332-338.
11. Caldú X., Vendrell P., Baries-Faz D., Clemente J., Bargalló N., Jurado M., Serran Grabulosa J., Junqué C. Impact of the COMT VaP 108/138 Met and DAT genotypes on prefrontal function in healthy subjects. Neuroimage 2007, 37:1437-1444.
12. Camps M., Cortes R., Gueye B., Probst A., Palacios J. Dopamine receptors in human brain: autoradiographic distribution of D2 sites. Neuroscience 1989, 28:275-290.
13. Clatworthy P., Lewis S., Brichard L., Hong Y., Izquierdo D., Clark L., Cools R., Acgirhio F., Baron J.-C., Fryer T., Robbins T. Dopamine release in dissociable striatal subregions predicts the different effects of oral methylphenidate on reversal learning and spatial working memory. J Neurosci 2009, 29:4690-4696.
14. Clementz B., Geyer M., Braff D. Multiple site evaluation of P50 suppression among schizophrenia and normal comparison subjects. Schizophr Res 1998, 30:71-80.
15. Cohen M., Krohn-Grimberghe A., Elger C., Weber B. Dopamine gene predicts the brain's response to dopaminergic drug. Eur J Neurosci 2007, 26:3652-3660.
16. Colzato L., Pratt J., Hommel B. Dopaminergic control of attentional flexibility: inhibition of return is associated with the dopamine transporter gene (DAT1). Front Hum Neurosci 2010, 4:1-6.
17. Cools R., Frank M., Gibbs S., Miyakawa A., Jagust W., D'Esposito M. Striatal dopamine predicts outcome-specific reversal learning and its sensitivity to dopaminergic drug administration. J Neurosci 2009, 29:1538-1543.
18. Cools R., D'Esposito M. The human striatum is necessary for responding to change in stimulus relevance. J Cogn Neurosci 2006, 18:1973-1983.
19. Cools R., Robbins T. Chemistry of the adaptive mind. Philos Transact A Math Phys Eng Sci 2004, 362:2871-2888.
20. Cools R. Role of dopamine in the motivational and cognitive control of behaviour. Neuroscientist 2008, 14:381-395.
21. Cornish K., Manly T., Savazo R., Swanson J., Morisano D., Butler N., Grant C., Cross G., Bentley L., Hollis C. Association of the dopamine transporter (DATI) 10/10-report genotype with ADHD symptoms and response inhibition in a general population sample. Mol Psychiatry 2005, 10:686-698.
22. Crawford H., McClain-Furmanski D., Castagnoli N., Castagnoli K. Enhancement of auditory sensory gating and stimulus-bound gamma band (40 Hz) oscillations in heavy tobacco smokers. Neurosci Lett 2002, 317:151-155.
23. Croft R., Dimoska A., Gonsalvez C., Clarke A. Suppression of P50 evoked potential component, schizotypal beliefs and smoking. Psychiatry Res 2004, 128:53-62.
24. Cromwell H., Woodward D. Inhibitory gating of single unit activity in amygdala: effects of ketamine, haloperidol, or nicotine. Biol Psychiatry 2007, 61:880-889.
25. Csomor P., Stadler R., Feldon J., Yeo B., Geyer M., Vollenweider F. Haloperidol differentially modulates prepulse inhibition and P50 suppression in healthy humans stratified for low and high gating levels. Neuropsychopharmacology 2007, 33:1-16.
26. De Wilde O., Bour L., Dingemans P., Koelman J., Linsses D. A meta-analysis of P50 studies in patients with schizophrenia and relatives: differences in methodology between research groups. Schizophr Res 2007, 97:137-151.
27. Dreher J., Kohn P., Kobchana B., Weinberger D., Berman K. Variation in dopamine genes influences responsivity of the human reward system. Proc Natl Acad Sci U S A 2009, 106:617-622.
28. Eysenck H., Eysenck S. Manual of the Eysenck personality questionnaire 1975, Educational and Testing Service, London.
29. Freedman R., Adler L., Waldo M., Pachtman E., Franks R. Neurophysiological evidence for a defect in inhibitory pathways in schizophrenia: comparison of medicated and drug-free patients. Biol Psychiatry 1983, 18:537-551.
30. Freedman R., Olincy A., Ross R., Waldo M., Stevens K., Adler L., Leonard S. The genetics of sensory gating deficits in schizophrenia. Curr Psychiatry Rep 2003, 5:155-161.
31. Fuerst D., Gallinat J., Boutros N. Range of sensory gating values and test-retest reliability in normal subjects. Psychophysiology 2007, 44:620-626.
32. Fuke S., Suo S., Takahashi N., Koike H., Sasagawa N., Ishiura S. The VNTR polymorphism of the human dopamine transporter (DATI) gene affects gene expression. Pharmacogenomics J 2001, 1:152-156.
33. Gainetdinov R., Jones S., Caron M. Functional hyperdopinergia in dopamine transporter knock-out mice. Biol Psychiatry 1999, 46:303-311.
34. Garcia-Garcia M., Barcelo F., Clemente J., Escera C. The role of the dopamine transporter DAT1 genotype on the neural correlates of cognitive flexibility. Eur J Neurosci 2010, 31:754-760.
35. Garcia-Garcia M., Barcelo R., Clemente J., Escera C. The role of DAT1 gene on the rapid detection of task novelty. Neuropsychologia 2010, 48:4136-4141.
36. Giros B., Mestikawy S., Godinot N., Zheng K., Han H., Yang-Feng T., Caron M. Cloning, pharmacological characterization, and chromosome assignment of the human dopamine transporter. Mol Pharmacol 1992, 42:383-390.
37. Gratton G., Coles M., Conchin E. A new method for off-line removal of ocular artifact. Electroencephalogr Clin Neurophysiol 1983, 55:468-484.
38. Grunwald T., Boutros N., Pezer N., Von Oertzen J., Fernandez G., Schaller C., Elger C. Neuronal substrates of sensory gating within the human brain. Biol Psychiatry 2003, 53:511-519.
39. Heinz A., Goldman D., Jones D., Palmour R., Hommer D., Gorey J., Lee K., Linnoila M., Weinberger D. Genotype influences in vivo dopamine transporter availability in human striatum. Neuropsychopharmacology 2000, 22:133-139.
40. Houston R., Stanford M. Mid-latency evoked potentials in self-reported impulsive aggression. Int J Psychophysiol 2001, 40:1-15.
41. Howes O., Kapur S. The dopamine hypotheses of schizophrenia: version III-the final common pathway. Schizophr Bull 2009, 35:549-562.
42. Hukkanen J., Jacob P., Benowitz N. Metabolism and disposition kinetics of nicotine. Pharmacol Rev 2005, 57:79-115.
43. Jacobsen L., Staley J., Zoghbl S., Selbyl J., Kosten T., Innis R., Gelertner J. Prediction of dopamine transporter binding availability by genotype: a preliminary report. Am J Psychiatry 2000, 157:1700-1703.
44. Jones S., Gainetdinov R., Jaber M., Giros B., Wightman R., Caron M. Profound neuronal plasticity in response to inactivation of the dopamine transporter. Proc Natl Acad Sci U S A 1998, 95:4029-4034.
45. Kang A., Palmatier M., Kidd K. Global variation of a 40-bp VNTR in the 3'-untranslated region of the dopamine transporter gene (SLC6A3). Biol Psychiatry 1999, 46:151-160.
46. Kapur S., Malmo D. Half a century of antipsychotics and still a central role for dopamine D2 receptors. Prog Neuropsychopharmacol Biol Psychiatry 2003, 27:1081-1090.
47. Kellendonck C., Simpson E., Polan N., Malleret C., Vronskaya S., Winiger V., Moore H., Kandel E. Transient and selective overexpression of dopamine D2 receptors in the striatum causes persistent abnormalities in prefrontal cortex functioning. Neuron 2006, 49:603-615.
48. Kenemans J., Kähkönen S. How human electrophysiology informs psychopharmacology: from bottom-up driven processing to top-down control. Neuropsychopharmacology 2011, 36:26-51.
49. Kim D., Szczypka M., Palmiter R. Dopamine-deficient mice are hypersensitive to dopamine receptor agonists. J Neurosci 2000, 20:4405-4413.
50. Knight R., Staines W., Swick D., Chao L. Prefrontal cortex regulates inhibition and excitation in distributed neural networks. Acta Psychol 1999, 101:159-178.
51. Knott V., Fisher D., Millar A. Differential effects of nicotine on P50 amplitude, its gating, and their neural sources in low and high suppressors. Neuroscience 2010, 170:816-826.
52. Knott V., Millar A., Fisher D. Sensory gating and source analysis of the auditory P50 in low and high suppressors. Neuroimage 2009, 44:992-1000.
53. Knott V., Millar A., Fisher D., Albert P. Effects of nicotine on the amplitude and gating of the auditory P50 and its influence by dopamine D2 receptor gene polymorphism. Neuroscience 2010, 166:145-156.
54. Krause K.-H., Dresel S., Krause J., La Fourgere C., Ackenheil M. The dopamine transporter and neuroimaging in attention deficit hyperactivity disorder. Neurosci Biobehav Rev 2003, 27:605-613.
55. Makela J., Hamaleinen M., Hari R., McEvoy L. Whole-head mapping of middle-latency auditory evoked magnetic fields. Electroencephalogr Clin Neurophysiol 1994, 92:414-421.
56. Metzger K., Maxwell C., Leang Y., Siegel S. Effects of nicotine vary across two auditory evoked potentials in the mouse. Biol Psychiatry 2007, 61:23-30.
57. Mill J., Asherson P., Browers C., D'Souza U., Crais J. Expression of the dopamine transporter gene is regulated by the 3' UTR VNTR: evidence from brain and lymphocytes using quantitative RT-PCR. Am J Med Genet 2002, 114:975-979.
58. Mitchell R., Howlett S., Earl L., White N., Crawford M., McComb J., Schanfield M., Briceno I., Papiha S., Osspova L., Crushits G., Leonard L., Crawford M. The distribution of the 3' VNTR polymorphism in the human dopamine transporter gene in world populations. Hum Biol 2000, 72:295-304.
59. Moxon K., Gerhardt G., Adler L. Dopaminergic modulation of the P50 auditory-evoked potential in a computer model of the CA3 region of the hippocampus: its relationship to sensory gating in schizophrenia. Biol Cybern 2003, 88:265-275.
60. Moxon K., Gerhardt G., Guilenllo M., Adler L. Inhibitory control of sensory gating in a computer model of the CA3 region of the hippocampus. Biol Cybern 2003, 88:247-264.
61. Nagamoto H., Adler L., Hea R., Griffith J., McRae K., Freedman R. Gating of auditory P50 in schizophrenics: unique effects of clozapine. Biol Psychiatry 1996, 40:181-188.
62. Nagamoto N., Adler L., McRae K., Huetti P., Cawthra E., Gerhardt G., Griffith J. Auditory P50 in schizophrenics on clozapine: improved gating parallels elevated improvement and changes in plasma 2-methoxy-4-hydroxyphenylglycol. Neuropsychobiology 1999, 39:10-17.
63. Olincy A., Harris J., Johnson L., Pender V., Kongs S., Allensworth D., Zerbe F., Leonard S., Stevens K., Stevens J., Martin L., Adler L., Soti F., Kem W., Freedman R. Proof-of-concept trial of an alpha7 nicotinic agonist in schizophrenia. Arch Gen Psychiatry 2006, 63:630-638.
64. Patterson J., Hetrick W., Boutros N., Jin Y., Sandman C., Stern H., Potkis S., Bunney W. P50 sensory gating ratios in schizophrenics and controls: a review and data analysis. Psychiatry Res 2008, 158:226-247.
65. Pelizzone M., Hari R., Makela J., Huttunen J., Ahlfors S., Hamalieyen M. Cortical origin of middle-latency auditory evoked responses. Neurosci Lett 1987, 82:303-307.
66. Phillips J., Ehrlichman R., Siegel S. Mecamylamine blocks nicotine-induced enhancement of the P20 auditory event-related potential and evoked gamma. Neuroscience 2007, 144:1314-1323.
67. Phillips A., Ahn S., Floresco S. Magnitude of dopamine release in medial prefrontal cortex predicts accuracy of memory on a delayed response task. J Neurosci 2004, 24:547-553.
68. Prata D., Mechelli A., Picchioni M., Fu C., Toulopoulou T., Bramon E., Walshe M., Murray R., Collier D., McGuire P. Altered effect of dopamine transporter 3' UTR VNTR genotype on prefrontal and striatal function in schizophrenia. Arch Gen Psychiatry 2009, 66:1162-1172.
69. Reite M., Teale P., Zimmerman J., Davis K., Whalen I. Source location of a 50 msec latency auditory evoked field component. Electroencephalogr Clin Neurophysiol 1988, 70:490-498.
70. Rentzsch J., Jackers-Scheruhl M., Boutros N., Gallinat J. Test-retest reliability of P50, N100 and P200 auditory sensory gating in healthy subjects. Int J Psychophysiol 2008, 57:81-90.
71. Rudnick N., Strasser A., Phillips J., Jepson C., Patterson F., Fry J., Turetsky B., Lerman C., Siegel S. Mouse model predicts effects of smoking and varenicline on event-related potentials in humans. Nicotine Tob Res 2010, 12:589-597.
72. Schmitt G., Frodl T., Dresel S., La Fougére C., Bottlender R., Koutsouleris N., Hahn K., Moller H., Meisenzahl E. Striatal dopamine transporter availability is associated with the productive psychotic state in first episode, drug-naive schizophrenic patients. Eur Arch Psychiatry Clin Neurosci 2006, 256:115-121.
73. Sesack S., Hawrylak V., Matus C., Guido M., Lovy A. Dopamine axon varicosities in the prelimbic division of the rat prefrontal cortex exhibit sparse immunoreactivity for the dopamine transporter. J Neurosci 1998, 18:2697-2708.
74. Simosky J., Stevens K., Adler L., Freedman R. Clozapine improves deficient inhibitory auditory processing in DBA/2 mice, via a nicotinic cholinergic mechanism. Psychopharmacology 2003, 165:386-396.
75. Simosky J., Stevens K., Kem W., Freedman R. Intragastric DMXB-A, an alpha7 nicotinic agonist, improves deficient sensory inhibition in DBA/2 mice. Biol Psychiatry 2001, 50:493-500.
76. Stevens K., Kem W., Mahnir V., Freedman R. Selective α7 nicotinic agonists normalize inhibition of auditory response in DBA mice. Psychopharmacology 1998, 136:320-327.
77. Stevens K., Kem W., Freedman R. Selective α7 nicotinic receptor stimulation normalizes chronic cocaine-induced loss of hippocampal sensory inhibition in C3H mice. Biol Psychiatry 1999, 46:1443-1450.
78. Stevens K., Freedman R., Collins A., Hail M. Genetic correlation of inhibitory gating of hippocampal auditory evoked response and alpha-bungarotoxin binding nicotine cholinergic receptors in inbred mouse strains. Neuropsychopharmacology 1996, 15:157-162.
79. Stevens K., Wear K. Normalizing effects of nicotine and a novel nicotinic agonist on hippocampal auditory gating in two animal models. Pharmacol Biochem Behav 1997, 57:869-874.
80. Vandenbergh C., Persico A., Hawkins A., Griffin C., Li X., Jabs E., Uhl G. Human dopamine transporter gene maps to chromosome 5p153 and displays a VNTR. Genomics 1992, 14:1104-1106.
81. Venables P. Input dysfunction in schizophrenia. Progress in experimental personality research 1964, 1-47. Academic Press, New York. B. Mabler (Ed.).
82. Wan L., Crawford H., Boutros N. P50 sensory gating: impact of high vs low schizotypal personality and smoking status. Int J Psychophysiol 2006, 60:1-9.
83. Wan L., Crawford H., Boutros N. Early and late auditory sensory: moderating influences from schizotypal personality, tobacco smoking status, and acute smoking. Psychiatry Res 2007, 151:11-20.
84. Weiss S., Tzavara E., Davis R., Nomikos C., McIntosh J., Giros B., Murtros M.-P. Functional alterations of nicotinic neurotransmission in dopamine transporter knock-out mice. Neuropharmacology 2007, 52:1496-1508.
85. Weisser R., Weisbrod M., Rouhrig M., Bupp A., Schroeder J., Sherg M. Is frontal lobe involved in the generation of auditory evoked P50?. Neuroreport 2001, 12:3303-3307.
86. Xu M., Ting Z., Li S., Zheng Y., Wu S., Gao R., Yu L., Guo T., Yang Y., Liu J., Zhang A., Zhao X., He G., Zhou J., Wang L., Xuan J., Du J., Li X., Feng G., Lin Z., Xu Y., St Clair P., Lin Z., He L. Pharmacogenetic effects of dopamine transporter gene polymorphisms on response to chlorpromazine and clozapine and on extrapyramidal syndrome in schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 2010, 34:1026-1032.
87. Yacubian J., Sommer T., Schroeder K., Gläscher J., Kalisch R., Levenberger B., Braus D., Buchel C. Gene-gene interaction associated with neural reward sensitivity. Proc Natl Acad Sci U S A 2007, 104:8125-8130.
88. Zhang X., Bearer E., Boulat B., Hall F., Uhl G., Jacobs R. Altered neurocircuitry in the dopamine transporter knockout mouse brain. PLoS One 2010, 5:e11506.
89. Zuckerman M. Behavioural expressions and biosocial bases of sensation seeking 1994, Cambridge University Press, Cambridge.