The effect of reduced dopamine D4 receptor expression in the 5-choice continuous performance task: Separating response inhibition from premature responding

Behavioural Brain Research

Volumn 222, Issue 1, 2011, Pages 183-192

  Young, Jared W ^a   Powell, Susan B ^a   Scott, Christine N ^a   Zhou, Xianjin ^a   Geyer, Mark A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

5 HT2C receptor; Attention; Dopamine D4 receptor; Impulsivity; Vigilance

Indexed keywords

ALERTNESS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTENTION; ATTENTION DISTURBANCE; CONTROLLED STUDY; DRD4 GENE; EXPLORATORY BEHAVIOR; GENE; GENE EXPRESSION; GENOTYPE; HETEROZYGOTE; IMPULSIVENESS; MALE; MENTAL PERFORMANCE; MOUSE; NONHUMAN; PREPULSE INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; STIMULUS RESPONSE; WILD TYPE;

AMINOPYRIDINES; ANALYSIS OF VARIANCE; ANIMALS; AROUSAL; ATTENTION; CHOICE BEHAVIOR; DOSE-RESPONSE RELATIONSHIP, DRUG; EXPLORATORY BEHAVIOR; GENE EXPRESSION; GENOTYPE; INDOLES; INHIBITION (PSYCHOLOGY); MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; NEUROPSYCHOLOGICAL TESTS; REACTION TIME; RECEPTORS, DOPAMINE D4; RNA, MESSENGER; SENSORY GATING; SEROTONIN ANTAGONISTS; STARTLE REACTION; STATISTICS AS TOPIC; TIME FACTORS;

EID: 79954578112     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.03.054     Document Type: Article

References (101)

1. Kaplan R.F., Stevens M. A review of adult ADHD: a neuropsychological and neuroimaging perspective. CNS Spectr 2002, 7:355-362.
2. Parasuraman R. The attentive brain 1998, MIT Press, Cambridge.
3. Riccio C.A., Reynolds C.R., Lowe P., Moore J.J. The continuous performance test: a window on the neural substrates for attention?. Arch Clin Neuropsychol 2002, 17:235-272.
4. Rosvold H., Sarason A.M.I., Bransome A.D.J., Beck L.H. A continuous performance test of brain damage. J Consult Psychol 1956, 20:343-350.
5. Conners C.K. The computerized continuous performance test. Psychopharmacol Bull 1985, 21:891-892.
6. Cornblatt B.A., Risch N.J., Faris G., Friedman D., Erlenmeyer-Kimling L. The Continuous Performance Test, identical pairs version (CPT-IP). I. New findings about sustained attention in normal families. Psychiatry Res 1988, 26:223-238.
7. Mackworth N.H. Researches on the measurement of human performance 1950, His Majesty's Stationery Office, London.
8. Carli M., Robbins T.W., Evenden J.L., Everitt B.J. Effects of lesions to ascending noradrenergic neurones on performance of a 5-choice serial reaction task in rats; implications for theories of dorsal noradrenergic bundle function based on selective attention and arousal. Behav Brain Res 1983, 9:361-380.
9. McGaughy J., Sarter M. Behavioral vigilance in rats: task validation and effects of age, amphetamine, and benzodiazepine receptor ligands. Psychopharmacology (Berl) 1995, 117:340-357.
10. Robbins T.W. The 5-choice serial reaction time task: behavioural pharmacology and functional neurochemistry. Psychopharmacology (Berl) 2002, 163:362-380.
11. Young J.W., Powell S.B., Risbrough V., Marston H.M., Geyer M.A. Using the MATRICS to guide development of a preclinical cognitive test battery for research in schizophrenia. Pharmacol Ther 2009, 122:150-202.
12. Young J.W., Light G.A., Marston H.M., Sharp R., Geyer M.A. The 5-choice continuous performance test: evidence for a translational test of vigilance for mice. PLoS One 2009, 4:e4227.
13. Groman S.M., James A.S., Jentsch J.D. Poor response inhibition: at the nexus between substance abuse and attention deficit/hyperactivity disorder. Neurosci Biobehav Rev 2009, 33:690-698.
14. Kuntsi J., McLoughlin G., Asherson P. Attention deficit hyperactivity disorder. Neuromol Med 2006, 8:461-484.
15. Crosbie J., Perusse D., Barr C.L., Schachar R.J. Validating psychiatric endophenotypes: inhibitory control and attention deficit hyperactivity disorder. Neurosci Biobehav Rev 2008, 32:40-55.
16. Bora E., Vahip S., Akdeniz F. Sustained attention deficits in manic and euthymic patients with bipolar disorder. Prog Neuropsychopharmacol Biol Psychiatry 2006, 30:1097-1102.
17. Greenwood T.A., Alexander M., Keck P.E., McElroy S., Sadovnick A.D., Remick R.A., et al. Segmental linkage disequilibrium within the dopamine transporter gene. Mol Psychiatry 2002, 7:165-173.
18. Barr C.L., Xu C., Kroft J., Feng Y., Wigg K., Zai G., et al. Haplotype study of three polymorphisms at the dopamine transporter locus confirm linkage to attention-deficit/hyperactivity disorder. Biol Psychiatry 2001, 49:333-339.
19. Waldman I.D., Rowe D.C., Abramowitz A., Kozel S.T., Mohr J.H., Sherman S.L., et al. Association and linkage of the dopamine transporter gene and attention-deficit hyperactivity disorder in children: heterogeneity owing to diagnostic subtype and severity. Am J Hum Genet 1998, 63:1767-1776.
20. Swanson J.M., Kinsbourne M., Nigg J., Lanphear B., Stefanatos G.A., Volkow N., et al. Etiologic subtypes of attention-deficit/hyperactivity disorder: brain imaging, molecular genetic and environmental factors and the dopamine hypothesis. Neuropsychol Rev 2007, 17:39-59.
21. Sunohara G.A., Roberts W., Malone M., Schachar R.J., Tannock R., Basile V.S., et al. Linkage of the dopamine D4 receptor gene and attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 2000, 39:1537-1542.
22. McCracken J.T., Smalley S.L., McGough J.J., Crawford L., Del'Homme M., Cantor R.M., et al. Evidence for linkage of a tandem duplication polymorphism upstream of the dopamine D4 receptor gene (DRD4) with attention deficit hyperactivity disorder (ADHD). Mol Psychiatry 2000, 5:531-536.
23. Barr C.L., Wigg K.G., Bloom S., Schachar R., Tannock R., Roberts W., et al. Further evidence from haplotype analysis for linkage of the dopamine D4 receptor gene and attention-deficit hyperactivity disorder. Am J Med Genet 2000, 96:262-267.
24. Kereszturi E., Kiraly O., Csapo Z., Tarnok Z., Gadoros J., Sasvari-Szekely M., et al. Association between the 120-bp duplication of the dopamine D4 receptor gene and attention deficit hyperactivity disorder: genetic and molecular analyses. Am J Med Genet B: Neuropsychiatr Genet 2007, 144B:231-236.
25. Muglia P., Petronis A., Mundo E., Lander S., Cate T., Kennedy J.L. Dopamine D4 receptor and tyrosine hydroxylase genes in bipolar disorder: evidence for a role of DRD4. Mol Psychiatry 2002, 7:860-866.
26. Asghari V., Sanyal S., Buchwaldt S., Paterson A., Jovanovic V., Van Tol H.H. Modulation of intracellular cyclic AMP levels by different human dopamine D4 receptor variants. J Neurochem 1995, 65:1157-1165.
27. D'Souza U.M., Russ C., Tahir E., Mill J., McGuffin P., Asherson P.J., et al. Functional effects of a tandem duplication polymorphism in the 5′flanking region of the DRD4 gene. Biol Psychiatry 2004, 56:691-697.
28. Schoots O., Van Tol H.H. The human dopamine D4 receptor repeat sequences modulate expression. Pharmacogenomics J 2003, 3:343-348.
29. Defagot M.C., Falzone T.L., Low M.J., Grandy D.K., Rubinstein M., Antonelli M.C. Quantitative analysis of the dopamine D4 receptor in the mouse brain. J Neurosci Res 2000, 59:202-208.
30. Khan Z.U., Gutierrez A., Martin R., Penafiel A., Rivera A., De La Calle A. Differential regional and cellular distribution of dopamine D2-like receptors: an immunocytochemical study of subtype-specific antibodies in rat and human brain. J Comp Neurol 1998, 402:353-371.
31. Chudasama Y., Robbins T.W. Psychopharmacological approaches to modulating attention in the five-choice serial reaction time task: implications for schizophrenia. Psychopharmacology (Berl) 2004, 174:86-98.
32. Fletcher P.J., Tampakeras M., Sinyard J., Higgins G.A. Opposing effects of 5-HT(2A) and 5-HT(2C) receptor antagonists in the rat and mouse on premature responding in the five-choice serial reaction time test. Psychopharmacology (Berl) 2007, 195:223-234.
33. Winstanley C.A., Dalley J.W., Theobald D.E., Robbins T.W. Fractionating impulsivity: contrasting effects of central 5-HT depletion on different measures of impulsive behavior. Neuropsychopharmacology 2004, 29:1331-1343.
34. Winstanley C.A., Theobald D.E., Dalley J.W., Glennon J.C., Robbins T.W. 5-HT2A and 5-HT2C receptor antagonists have opposing effects on a measure of impulsivity: interactions with global 5-HT depletion. Psychopharmacology (Berl) 2004, 176:376-385.
35. Puumala T., Sirvio J. Changes in activities of dopamine and serotonin systems in the frontal cortex underlie poor choice accuracy and impulsivity of rats in an attention task. Neuroscience 1998, 83:489-499.
36. Graham S., Ho M.Y., Bradshaw C.M., Szabadi E. Facilitated acquisition of a temporal discrimination following destruction of the ascending 5-hydroxytryptaminergic pathways. Psychopharmacology (Berl) 1994, 116:373-378.
37. Asgari K., Body S., Bak V.K., Zhang Z.Q., Rickard J.F., Glennon J.C., et al. Effects of 5-HT2A receptor stimulation on the discrimination of durations by rats. Behav Pharmacol 2006, 17:51-59.
38. Hershey T., Black K.J., Hartlein J., Braver T.S., Barch D.M., Carl J.L., et al. Dopaminergic modulation of response inhibition: an fMRI study. Brain Res Cogn Brain Res 2004, 20:438-448.
39. Cropley V.L., Fujita M., Innis R.B., Nathan P.J. Molecular imaging of the dopaminergic system and its association with human cognitive function. Biol Psychiatry 2006, 59:898-907.
40. Perry W., Minassian A., Henry B., Kincaid M., Young J.W., Geyer M.A. Quantifying over-activity in bipolar and schizophrenia patients in a human open field paradigm. Psychiatry Res 2010, 178:84-91.
41. Perry W., Minassian A., Paulus M.P., Young J.W., Kincaid M.J., Ferguson E.J., et al. A reverse-translational study of dysfunctional exploration in psychiatric disorders: from mice to men. Arch Gen Psychiatry 2009, 66:1072-1080.
42. Young J.W., Goey A.K., Minassian A., Perry W., Paulus M.P., Geyer M.A. GBR 12909 administration as a mouse model of bipolar disorder mania: mimicking quantitative assessment of manic behavior. Psychopharmacology (Berl) 2010, 208:443-454.
43. Young J.W., Goey A.K., Minassian A., Perry W., Paulus M.P., Geyer M.A. The mania-like exploratory profile in genetic dopamine transporter mouse models is diminished in a familiar environment and reinstated by subthreshold psychostimulant administration. Pharmacol Biochem Behav 2010, 96:7-15.
44. Young J.W., Minassian A., Paulus M.P., Geyer M.A., Perry W. A reverse-translational approach to bipolar disorder: rodent and human studies in the Behavioral Pattern Monitor. Neurosci Biobehav Rev 2007, 31:882-896.
45. Braff D., Stone C., Callaway E., Geyer M., Glick I., Bali L. Prestimulus effects on human startle reflex in normals and schizophrenics. Psychophysiology 1978, 15:339-343.
46. Geyer M.A. The family of sensorimotor gating disorders: comorbitities or diagnostic overlaps. Neurotox Res 2006, 10:211-220.
47. Geyer M.A. Developing translational animal models for symptoms of schizophrenia or bipolar mania. Neurotox Res 2008, 14:71-78.
48. Perry W., Minassian A., Feifel D., Braff D.L. Sensorimotor gating deficits in bipolar disorder patients with acute psychotic mania. Biol Psychiatry 2001, 50:418-424.
49. Swerdlow N.R., Taaid N., Oostwegel J.L., Randolph E., Geyer M.A. Towards a cross-species pharmacology of sensorimotor gating: effects of amantadine, bromocriptine, pergolide and ropinirole on prepulse inhibition of acoustic startle in rats. Behav Pharmacol 1998, 9:389-396.
50. Paulus M., Minassian A., Masten V., Feifel D., Geyer M., Perry W. Human Behavioral Pattern Monitor differentiates activity patterns of bipolar manic and attention deficit hyperactivity subjects. Biol Psychiatr 2007, 61:227S.
51. Feifel D., Minassian A., Perry W. Prepulse inhibition of startle in adults with ADHD. J Psychiatr Res 2009, 43:484-489.
52. Hawk L.W., Yartz A.R., Pelham W.E., Lock T.M. The effects of methylphenidate on prepulse inhibition during attended and ignored prestimuli among boys with attention-deficit hyperactivity disorder. Psychopharmacology (Berl) 2003, 165:118-127.
53. Castellanos F.X., Fine E.J., Kaysen D., Marsh W.L., Rapoport J.L., Hallett M. Sensorimotor gating in boys with Tourette's syndrome and ADHD: preliminary results. Biol Psychiatry 1996, 39:33-41.
54. Rubinstein M., Phillips T.J., Bunzow J.R., Falzone T.L., Dziewczapolski G., Zhang G., et al. Mice lacking dopamine D4 receptors are supersensitive to ethanol, cocaine, and methamphetamine. Cell 1997, 90:991-1001.
55. Young J.W., Finlayson K., Spratt C., Marston H.M., Crawford N., Kelly J.S., et al. Nicotine improves sustained attention in mice: evidence for involvement of the alpha7 nicotinic acetylcholine receptor. Neuropsychopharmacology 2004, 29:891-900.
56. Green D.M., Swets J.A. Signal detection theory and psychophysics 1966, Wiley & Sons, New York.
57. McNicol D. A primer of signal detection theory 1972, George, Allen & Unwin, London.
58. Frey P.W., Colliver J.A. Sensitivity and responsibility measures for discrimination learning. Learn Motiv 1973, 4:327-342.
59. Marston H.M. Analysis of cognitive function in animals, the value of SDT. Brain Res Cogn Brain Res 1996, 3:269-277.
60. Sahgal A. Some limitations of indices derived from signal detection theory: evaluation of an alternative index for measuring bias in memory tasks. Psychopharmacology (Berl) 1987, 91:517-520.
61. Young J.W., Crawford N., Kelly J.S., Kerr L.E., Marston H.M., Spratt C., et al. Impaired attention is central to the cognitive deficits observed in alpha 7 deficient mice. Eur Neuropsychopharmacol 2007, 17:145-155.
62. Halberstadt A.L., van der Heijden I., Ruderman M.A., Risbrough V.B., Gingrich J.A., Geyer M.A., et al. 5-HT(2A) and 5-HT(2C) receptors exert opposing effects on locomotor activity in mice. Neuropsychopharmacology 2009, 34:1958-1967.
63. Risbrough V.B., Masten V.L., Caldwell S., Paulus M.P., Low M.J., Geyer M.A. Differential contributions of dopamine D(1), D(2), and D(3) receptors to MDMA-induced effects on locomotor behavior patterns in mice. Neuropsychopharmacology 2006, 31:2349-2358.
64. Geyer M.A., Russo P.V., Masten V.L. Multivariate assessment of locomotor behavior: pharmacological and behavioral analyses. Pharmacol Biochem Behav 1986, 25:277-288.
65. Paulus M.P., Geyer M.A. A temporal and spatial scaling hypothesis for the behavioral effects of psychostimulants. Psychopharmacology (Berl) 1991, 104:6-16.
66. Geyer M.A., Swerdlow N.R., Mansbach R.S., Braff D.L. Startle response models of sensorimotor gating and habituation deficits in schizophrenia. Brain Res Bull 1990, 25:485-498.
67. Helms C.M., Gubner N.R., Wilhelm C.J., Mitchell S.H., Grandy D.K. D4 receptor deficiency in mice has limited effects on impulsivity and novelty seeking. Pharmacol Biochem Behav 2008, 90:387-393.
68. Thanos P.K., Habibi R., Michaelides M., Patel U.B., Suchland K., Anderson B.J., et al. Dopamine D4 receptor (D4R) deletion in mice does not affect operant responding for food or cocaine. Behav Brain Res 2010, 207:508-511.
69. Thanos P., Bermeo C., Rubinstein M., Suchland K., Wang G., Grandy D., et al. Conditioned place preference and locomotor activity in response to methylphenidate, amphetamine and cocaine in mice lacking dopamine D4 receptors. J Psychopharmacol 2009.
70. Epstein J.N., Erkanli A., Conners C.K., Klaric J., Costello J.E., Angold A. Relations between Continuous Performance Test performance measures and ADHD behaviors. J Abnorm Child Psychol 2003, 31:543-554.
71. Levy F., Hobbes G. Discrimination of attention deficit hyperactivity disorder by the continuous performance test. J Paediatr Child Health 1997, 33:384-387.
72. Monuteaux M.C., Seidman L.J., Faraone S.V., Makris N., Spencer T., Valera E., et al. A preliminary study of dopamine D4 receptor genotype and structural brain alterations in adults with ADHD. Am J Med Genet B: Neuropsychiatr Genet 2008, 147B:1436-1441.
73. Delawalla Z., Csernansky J.G., Barch D.M. Prefrontal cortex function in nonpsychotic siblings of individuals with schizophrenia. Biol Psychiatry 2008, 63:490-497.
74. Yoon J.H., Minzenberg M.J., Ursu S., Ryan Walter B.S., Wendelken C., Ragland J.D., et al. Association of dorsolateral prefrontal cortex dysfunction with disrupted coordinated brain activity in schizophrenia: relationship with impaired cognition, behavioral disorganization, and global function. Am J Psychiatry 2008, 165:1006-1014.
75. Rubinstein M., Cepeda C., Hurst R.S., Flores-Hernandez J., Ariano M.A., Falzone T.L., et al. Dopamine D4 receptor-deficient mice display cortical hyperexcitability. J Neurosci 2001, 21:3756-3763.
76. Thomas T.C., Grandy D.K., Gerhardt G.A., Glaser P.E. Decreased dopamine D4 receptor expression increases extracellular glutamate and alters its regulation in mouse striatum. Neuropsychopharmacology 2009, 34:436-445.
77. Wang H.D., Stanwood G.D., Grandy D.K., Deutch A.Y. Dystrophic dendrites in prefrontal cortical pyramidal cells of dopamine D1 and D2 but not D4 receptor knockout mice. Brain Res 2009, 1300:58-64.
78. Hoerst M., Weber-Fahr W., Tunc-Skarka N., Ruf M., Bohus M., Schmahl C., et al. Correlation of glutamate levels in the anterior cingulate cortex with self-reported impulsivity in patients with borderline personality disorder and healthy controls. Arch Gen Psychiatry 2010, 67:946-954.
79. Dulawa S.C., Grandy D.K., Low M.J., Paulus M.P., Geyer M.A. Dopamine D4 receptor-knock-out mice exhibit reduced exploration of novel stimuli. J Neurosci 1999, 19:9550-9556.
80. Ralph R.J., Varty G.B., Kelly M.A., Wang Y.M., Caron M.G., Rubinstein M., et al. The dopamine D2, but not D3 or D4, receptor subtype is essential for the disruption of prepulse inhibition produced by amphetamine in mice. J Neurosci 1999, 19:4627-4633.
81. Ornitz E.M., Hanna G.L., de Traversay J. Prestimulation-induced startle modulation in attention-deficit hyperactivity disorder and nocturnal enuresis. Psychophysiology 1992, 29:437-451.
82. Perry W., Minassian A., Paulus M.P., Young J.W., Kincaid M.J., Ferguson E.J., et al. A reverse-translational study of dysfunctional exploration in psychiatric disorders: from mice to men. Arch Gen Psychiatry 2009, 60:1072-1080.
83. Taylor E. Clinical foundations of hyperactivity research. Behav Brain Res 1998, 94:11-24.
84. Wilens T.E., Biederman J., Faraone S.V., Martelon M., Westerberg D., Spencer T.J. Presenting ADHD symptoms, subtypes, and comorbid disorders in clinically referred adults with ADHD. J Clin Psychiatry 2009, 70:1557-1562.
85. Giros B., Jaber M., Jones S.R., Wightman R.M., Caron M.G. Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature 1996, 379:606-612.
86. Viggiano D., Ruocco L.A., Sadile A.G. Dopamine phenotype and behaviour in animal models: in relation to attention deficit hyperactivity disorder. Neurosci Biobehav Rev 2003, 27:623-637.
87. Shaywitz B.A., Yager R.D., Klopper J.H. Selective brain dopamine depletion in developing rats: an experimental model of minimal brain dysfunction. Science 1976, 191:305-308.
88. Kostrzewa R.M., Kostrzewa J.P., Kostrzewa R.A., Nowak P., Brus R. Pharmacological models of ADHD. J Neural Transm 2008, 115:287-298.
89. Sagvolden T., Johansen E.B., Woien G., Walaas S.I., Storm-Mathisen J., Bergersen L.H., et al. The spontaneously hypertensive rat model of ADHD-the importance of selecting the appropriate reference strain. Neuropharmacology 2009, 57:619-626.
90. Cannon T.D., Keller M.C. Endophenotypes in the genetic analyses of mental disorders. Annu Rev Clin Psychol 2006, 2:267-290.
91. Balanza-Martinez V., Rubio C., Selva-Vera G., Martinez-Aran A., Sanchez-Moreno J., Salazar-Fraile J., et al. Neurocognitive endophenotypes (endophenocognitypes) from studies of relatives of bipolar disorder subjects: a systematic review. Neurosci Biobehav Rev 2008, 32:1426-1438.
92. Turetsky B.I., Calkins M.E., Light G.A., Olincy A., Radant A.D., Swerdlow N.R. Neurophysiological endophenotypes of schizophrenia: the viability of selected candidate measures. Schizophr Bull 2007, 33:69-94.
93. Aron A.R., Poldrack R.A. Cortical and subcortical contributions to Stop signal response inhibition: role of the subthalamic nucleus. J Neurosci 2006, 26:2424-2433.
94. Chen W.J., Faraone S.V. Sustained attention deficits as markers of genetic susceptibility to schizophrenia. Am J Med Genet 2000, 97:52-57.
95. Dalley J.W., Theobald D.E., Eagle D.M., Passetti F., Robbins T.W. Deficits in impulse control associated with tonically-elevated serotonergic function in rat prefrontal cortex. Neuropsychopharmacology 2002, 26:716-728.
96. Passetti F., Dalley J.W., O'Connell M.T., Everitt B.J., Robbins T.W. Increased acetylcholine release in the rat medial prefrontal cortex during performance of a visual attentional task. Eur J Neurosci 2000, 12:3051-3058.
97. Evenden J. Impulsivity: a discussion of clinical and experimental findings. J Psychopharmacol 1999, 13:180-192.
98. Evenden J.L. Varieties of impulsivity. Psychopharmacology (Berl) 1999, 146:348-361.
99. Grottick A.J., Higgins G.A. Assessing a vigilance decrement in aged rats: effects of pre-feeding, task manipulation, and psychostimulants. Psychopharmacology (Berl) 2002, 164:33-41.
100. Woolley M.L., Waters K.A., Reavill C., Bull S., Lacroix L.P., Martyn A.J., et al. Selective dopamine D4 receptor agonist (A-412997) improves cognitive performance and stimulates motor activity without influencing reward-related behaviour in rat. Behav Pharmacol 2008, 19:765-776.
101. Browman K.E., Curzon P., Pan J.B., Molesky A.L., Komater V.A., Decker M.W., et al. A-412997, a selective dopamine D4 agonist, improves cognitive performance in rats. Pharmacol Biochem Behav 2005, 82:148-155.