Reverse translation of the rodent 5C-CPT reveals that the impaired attention of people with schizophrenia is similar to scopolamineinduced deficits in mice

Translational Psychiatry

Volumn 3, Issue , 2013, Pages

  Young, J W ^a,b   Geyer, M A ^a,b   Rissling, A J ^a   Sharp, R F ^a   Eyler, L T ^a,b   Asgaard, G L ^c   Light, G A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Veteran's Affairs   (United States)

^c NAVAL MEDICAL CENTER PORTSMOUTH   (United States)

Author keywords

Attention; Mice; Schizophrenia; Scopolamine; Translation; Vigilance

Indexed keywords

SCOPOLAMINE; MUSCARINIC RECEPTOR BLOCKING AGENT; SCOPOLAMINE BROMIDE;

5 CHOICE CONTINUOUS PERFORMANCE TEST; ACCURACY; ADULT; ALERTNESS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATTENTION DISTURBANCE; CLINICAL ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; FEMALE; HUMAN; IMPULSIVENESS; MALE; MIDDLE AGED; MOUSE; NONHUMAN; PSYCHOLOGIC TEST; REACTION TIME; SCHIZOPHRENIA; ANIMAL; ATTENTION; CHEMICALLY INDUCED DISORDER; DISEASE MODEL; NEUROPSYCHOLOGICAL TEST; PATHOPHYSIOLOGY; PSYCHOLOGY; YOUNG ADULT;

ADULT; ANIMALS; ATTENTION; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALE; MICE; MIDDLE AGED; MUSCARINIC ANTAGONISTS; NEUROPSYCHOLOGICAL TESTS; REACTION TIME; SCHIZOPHRENIA; SCHIZOPHRENIC PSYCHOLOGY; SCOPOLAMINE HYDROBROMIDE; YOUNG ADULT;

EID: 84884307706     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2013.82     Document Type: Article

References (99)

1. Keefe RS, Bilder RM, Davis SM, Harvey PD, Palmer BW, Gold JM et al. Neurocognitive effects of antipsychotic medications in patients with chronic schizophrenia in the CATIE Trial. Arch Gen Psychiatry 2007; 64: 633-647.
2. Mintz J, Kopelowicz A. CUtLASS confirms CATIE. Arch Gen Psychiatry 2007; 64: 978 author reply 9-80.
3. Parks JJ, Radke AQ, Tandon R. Impact of the CATIE findings on state mental health policy. Psychiatr Serv 2008; 59: 534-536.
4. Green MF. What are the functional consequences of neurocognitive deficits in schizophrenia? Am J Psychiatry 1996; 153: 321-330.
5. Green MF, Nuechterlein KH, Kern RS, Baade LE, Fenton WS, Gold JM et al. Functional co-primary measures for clinical trials in schizophrenia: results from the MATRICS Psychometric and Standardization Study. Am J Psychiatry 2008; 165: 221-228.
6. Geyer MA, Olivier B, Joels M, Kahn RS. From antipsychotic to anti-schizophrenia drugs: role of animal models. Trends Pharmacol Sci 2012; 33: 515-521.
7. Floresco SB, Geyer MA, Gold LH, Grace AA. Developing predictive animal models and establishing a preclinical trials network for assessing treatment effects on cognition in schizophrenia. Schizophr Bull 2005; 31: 888-894.
8. Sarter M. Animal cognition: defining the issues. Neurosci Biobehav Rev. 2004; 28: 645-650.
9. Kraepelin E. Dementia Praecox and Paraphrenology. E&S Livingston: Edinburgh, UK, 1919.
10. Bleuler E. Dementia Praecox or the Group of Schizophrenias. International Universities Press: New York, NY, 1950.
11. Marder SR. The NIMH-MATRICS project for developing cognition-enhancing agents for schizophrenia. Dialogues Clin Neurosci 2006; 8: 109-113.
12. Marder SR, Fenton W. Measurement and Treatment Research to Improve Cognition in Schizophrenia: NIMH MATRICS initiative to support the development of agents for improving cognition in schizophrenia. Schizophr Res 2004; 72: 5-9.
13. Carter CS, Barch DM. Cognitive neuroscience-based approaches to measuring and improving treatment effects on cognition in schizophrenia: the CNTRICS initiative. Schizophr Bull 2007; 33: 1131-1137.
14. Barch DM, Carter CS, Arnsten A, Buchanan RW, Cohen JD, Geyer M et al. Selecting paradigms from cognitive neuroscience for translation into use in clinical trials: proceedings of the third CNTRICS meeting. Schizophr Bull 2009; 35: 109-114.
15. Geyer MA. New opportunities in the treatment of cognitive impairments associated with schizophrenia. Curr Dir Psychol Sci 2010; 19: 264-269.
16. Young JW, Powell SB, Risbrough V, Marston HM, Geyer MA. Using the MATRICS to guide development of a preclinical cognitive test battery for research in schizophrenia. Pharmacol Ther 2009; 122: 150-202.
17. Salgado-Pineda P, Baeza I, Perez-Gomez M, Vendrell P, Junque C, Bargallo N et al. Sustained attention impairment correlates to gray matter decreases in first episode neuroleptic-naive schizophrenic patients. Neuroimage 2003; 19(2 Pt 1): 365-375.
18. Kleinlogel H, Strik W, Begre S. Increased NoGo-anteriorisation in first-episode schizophrenia patients during Continuous Performance Test. Clin Neurophysiol 2007; 118: 2683-2691.
19. Cornblatt BA, Keilp JG. Impaired attention, genetics, and the pathophysiology of schizophrenia. Schizophr Bull. 1994; 20: 31-46.
20. Nuechterlein KH, Luck SJ, Lustig C, Sarter M. CNTRICS final task selection: control of attention. Schizophr Bull 2009; 35: 182-196.
21. Ko SY, Chen PS, Yang YK, Liao YC, Lee YD, Yeh TL et al. Correlation between performance on the Continuous Performance Test and economic costs in patients with schizophrenia. Psychiatry Clin Neurosci 2003; 57: 373-377.
22. Silverstein SM, Light G, Palumbo DR. The sustained attention test: a measure of attentional disturbance. Computers in Human Behavior 1998; 14: 463.
23. Borgaro S, Pogge DL, DeLuca VA, Bilginer L, Stokes J, Harvey PD. Convergence of different versions of the continuous performance test: clinical and scientific implications. J Clin Exp Neuropsychol 2003; 25: 283-292.
24. Mackworth NH. Researches on the Measurement of Human Performance. His Majesty's Stationery Office: London, 1950.
25. Parasuraman R. The Attentive Brain. MIT Press: Cambridge, 1998.
26. Nuechterlein KH. Vigilance in schizoprhenia and related disorders. In: Steinhauer SR, Gruzelier JH, Zubin J (eds). Neuropsychology, Pscyhophysiology, and Information Processing Handbook of Schizophrenia. Elsevier Science: New York, 1991, pp 397-433.
27. Lustig C, Kozak R, Sarter M, Young JW, Robbins TW. CNTRICS final animal model task selection: Control of attention. Neurosci Biobehav Rev 2012 (e-pub ahead of print).
28. Morris R, Evenden J, Sahakian B, Robbins T. Computer aided assessment of dementia: comparative studies of neuropsychological deficits in Alzheimer's type dementia and Parkinson's disease. In: Stahl S, Iversen S, Goodman E (eds). Cognitive Neurochemistry. Oxford University Press: Oxford, 1987, pp 21-36.
29. Demeter E, Sarter M, Lustig C. Rats and humans paying attention: cross-species task development for translational research. Neuropsychology 2008; 22: 787-799.
30. Riccio CA, Reynolds CR, Lowe P, Moore JJ. The continuous performance test: a window on the neural substrates for attention? Arch Clin Neuropsychol 2002; 17: 235-272.
31. Barnes SA, Young JW, Neill JC. D(1) receptor activation improves vigilance in rats as measured by the 5-choice continuous performance test. Psychopharmacology (Berl) 2011; 220: 129-141.
32. Barnes SA, Young JW, Neill JC. Rats tested after a washout period from subchronic PCP administration exhibited impaired performance in the 5-Choice Continuous Performance Test (5C-CPT) when the attentional load was increased. Neuropharmacology 2011; 62: 1432-1441.
33. Young JW, Light GA, Marston HM, Sharp R, Geyer MA. The 5-choice continuous performance test: evidence for a translational test of vigilance for mice. PLoS One 2009; 4: e4227.
34. Young JW, Powell SB, Scott CN, Zhou X, Geyer MA. The effect of reduced dopamine D4 receptor expression in the 5-choice continuous performance task: separating response inhibition from premature responding. Behav Brain Res 2011; 222: 183-192.
35. Rund BR, Orbeck AL, Landro NI. Vigilance deficits in schizophrenics and affectively disturbed patients. Acta Psychiatr Scand 1992; 86: 207-212.
36. Bedwell JS, Kamath V, Baksh E. Comparison of three computer-administered cognitive tasks as putative endophenotypes of schizophrenia. Schizophr Res 2006; 88: 36-46.
37. Hasenkamp W, Kelley M, Egan G, Green A, Wilcox L, Boshoven W et al. Lack of relationship between acoustic startle and cognitive variables in schizophrenia and control subjects. Psychiatry Res 2011; 187: 324-328.
38. Lysaker PH, Tsai J, Henninger LL, Vohs JL, Viverito K. Decrements in sustained attention across trials in a continuous performance test: associations with social functioning in schizophrenia. J Nerv Ment Dis 2010; 198: 154-158.
39. Nestor PG, Faux SF, McCarley RW, Shenton ME, Sands SF. Measurement of visual sustained attention in schizophrenia using signal detection analysis and a newly developed computerized CPT task. Schizophr Res 1990-Dec 3: 329-332.
40. Nestor PG, Faux SF, McCarley RW, Sands SF, Horvath TB, Peterson A. Neuroleptics improve sustained attention in schizophrenia. A study using signal detection theory. Neuropsychopharmacology 1991; 4: 145-149.
41. Nuechterlein KH. Signal detection in vigilance tasks and behavioral attributes among offspring of schizophrenic mothers and among hyperactive children. J Abnorm Psychol 1983; 92: 4-28.
42. Raedler TJ. Comparison of the in-vivo muscarinic cholinergic receptor availability in patients treated with clozapine and olanzapine. Int J Neuropsychopharmacol 2007; 10: 275-280.
43. Sarter M, Lustig C, Taylor SF. Cholinergic contributions to the cognitive symptoms of schizophrenia and the viability of cholinergic treatments. Neuropharmacology 2012; 62: 1544-1553.
44. Takahashi H, Rissling AJ, Pascual-Marqui R, Kirihara K, Pela M, Sprock J et al. Neural substrates of normal and impaired preattentive sensory discrimination in large cohorts of nonpsychiatric subjects and schizophrenia patients as indexed by MMN and P3a change detection responses. Neuroimage 2012; 66C: 594-603.
45. Rissling AJ, Braff DL, Swerdlow NR, Hellemann G, Rassovsky Y, Sprock J et al. Disentangling early sensory information processing deficits in schizophrenia. Clin Neurophysiol 2012; 123: 1942-1949.
46. First M, Spitzer R, Gibbon M, Williams J. Structured Clinical Interview for DSMIV Axis 1. Disorders - Patient Edition. New York State Psychiatric Institute: New York, 1995.
47. Andreasen NC. Scale for the Assessment of Negative Symptoms (SANS). University of Iowa: Iowa City, 1983.
48. Andreasen NC. Scale for the Assessment of Positive Symptoms (SAPS). University of Iowa: Iowa City, 1984.
49. Hall RC. Global assessment of funcitoning; a modified scale. Pscyhosomatics 1995; 36: 267-275.
50. Edgar JC, Hunter MA, Huang M, Smith AK, Chen Y, Sadek J et al. Termporal and frontal cortical thickness associations with M100 auditory gating and attention in healthy controls and individuals with schizophrenia. Schiz Res 2012; 140: 250-257.
51. Krakvik B, Stiles T, Hugdhal K. Experiencing malevolent voices is associated with attentional dysfunction in psychotic patients. Scand J Psychol 2013; 54: 72-77.
52. Green DM, Swets JA. Signal Detection Theory and Psychophysics. Wiley & Sons: New York, 1966.
53. McNicol D. A Primer of Signal Detection Theory. George Allen & Unwin: London, 1972.
54. Frey PW, Colliver JA. Sensitivity and responsibility measures for discrimination learning. Learn Motiv 1973; 4: 327-342.
55. Marston HM. Analysis of cognitive function in animals, the value of SDT. Brain Res Cogn Brain Res 1996; 3: 269-277.
56. 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.
57. Young JW, Finlayson K, Spratt C, Marston HM, Crawford N, Kelly JS et al. Nicotine improves sustained attention in mice: evidence for involvement of the alpha7 nicotinic acetylcholine receptor. Neuropsychopharmacology 2004; 29: 891-900.
58. Young JW, Meves JM, Geyer MA. Nicotinic agonist-induced improvement of vigilance in mice in the 5-choice continuous performance test. Behav Brain Res 2013; 240: 119-133.
59. Redrobe JP, Nielsen EO, Christensen JK, Peters D, Timmermann DB, Olsen GM. Alpha7 nicotinic acetylcholine receptor activation ameliorates scopolamine- induced behavioural changes in a modified continuous Y-maze task in mice. Eur J Pharmacol 2009; 602: 58-65.
60. de Bruin NM, Fransen F, Duytschaever H, Grantham C, Megens AA. Attentional performance of (C57BL/6Jx129Sv)F2 mice in the five-choice serial reaction time task. Physiol Behav 2006; 89: 692-703.
61. Humby T, Laird FM, Davies W, Wilkinson LS. Visuospatial attentional functioning in mice: interactions between cholinergic manipulations and genotype. Eur J Neurosci 1999; 11: 2813-2823.
62. Pattij T, Janssen MC, Loos M, Smit AB, Schoffelmeer AN, van Gaalen MM. Strain specificity and cholinergic modulation of visuospatial attention in three inbred mouse strains. Genes Brain Behav 2007; 6: 579-587.
63. Mussgay L, Hertwig R. Signal detection indices in schizophrenics on a visual, auditory, and bimodal Continuous Performance Test. Schizophr Res 1990; 3: 303-310.
64. Rutschmann J, Cornblatt B, Erlenmeyer-Kimling L. Sustained attention in children at risk for schizophrenia. Report on a continuous performance test. Arch Gen Psychiatry 1977; 34: 571-575.
65. Depatie L, O'Driscoll GA, Holahan AL, Atkinson V, Thavundayil JX, Kin NN et al. Nicotine and behavioral markers of risk for schizophrenia: a double-blind, placebo-controlled, cross-over study. Neuropsychopharmacology 2002; 27: 1056-1070.
66. Hasenkamp W, James GA, Boshoven W, Duncan E. Altered engagement of attention and default networks during target detection in schizophrenia. Schizophr Res 2011; 125: 169-173.
67. Hahn B, Robinson BM, Kaiser ST, Matveeva TM, Harvey AN, Luck SJ et al. Kraepelin and Bleuler had it right: people with schizophrenia have deficits sustaining attention over time. J Abnorm Psychol 2012; 121: 641-648.
68. Riccio CA, Waldrop JJ, Reynolds CR, Lowe P. Effects of stimulants on the continuous performance test (CPT): implications for CPT use and interpretation. J Neuropsychiatry Clin Neurosci 2001; 13: 326-335.
69. Bedard AC, Ickowicz A, Logan GD, Hogg-Johnson S, Schachar R, Tannock R. Selective inhibition in children with attention-deficit hyperactivity disorder off and on stimulant medication. J Abnorm Child Psychol 2003; 31: 315-327.
70. Wada N, Yamashita Y, Matsuishi T, Ohtani Y, Kato H. The test of variables of attention (TOVA) is useful in the diagnosis of Japanese male children with attention deficit hyperactivity disorder. Brain Dev 2000; 22: 378-382.
71. Huang YS, Chao CC, Wu YY, Chen YY, Chen CK. Acute effects of methylphenidate on performance during the Test of Variables of Attention in children with attention deficit/hyperactivity disorder. Psychiatry Clin Neurosci 2007; 61: 219-225.
72. Ozan E, Deveci E, Oral M, Karahan U, Oral E, Aydin N et al. Neurocognitive functioning in a group of offspring genetically at high-risk for schizophrenia in Eastern Turkey. Brain Res Bull 2010; 82: 218-223.
73. McDowell JE, Clementz BA. Ocular-motor delayed-response task performance among schizophrenia patients. Neuropsychobiology 1996; 34: 67-71.
74. Barnett JH, Robbins TW, Leeson VC, Sahakian BJ, Joyce EM, Blackwell AD. Assessing cognitive function in clinical trials of schizophrenia. Neurosci Biobehav Rev 2010; 34: 1161-1177.
75. Chouinard S, Stip E, Poulin J, Melun JP, Godbout R, Guillem F et al. Rivastigmine treatment as an add-on to antipsychotics in patients with schizophrenia and cognitive deficits. Curr Med Res Opin 2007; 23: 575-583.
76. Fagerlund B, Soholm B, Fink-Jensen A, Lublin H, Glenthoj BY. Effects of donepezil adjunctive treatment to ziprasidone on cognitive deficits in schizophrenia: a double-blind, placebo-controlled study. Clin Neuropharmacol 2007; 30: 3-12.
77. Nelson EB, Sax KW, Strakowski SM. Attentional performance in patients with psychotic and nonpsychotic major depression and schizophrenia. Am J Psychiatry 1998; 155: 137-139.
78. Pandurangi AK, Sax KW, Pelonero AL, Goldberg SC. Sustained attention and positive formal thought disorder in schizophrenia. Schizophr Res 1994; 13: 109-116.
79. Liu SK, Hwu HG, Chen WJ. Clinical symptom dimensions and deficits on the Continuous Performance Test in schizophrenia. Schizophr Res 1997; 25: 211-219.
80. Marks MJ, O'Connor MF, Artman LD, Burch JB, Collins AC. Chronic scopolamine treatment and brain cholinergic function. Pharmacol Biochem Behav 1984; 20: 771-777.
81. Lenz RA, Baker JD, Locke C, Rueter LE, Mohler EG, Wesnes K et al. The scopolamine model as a pharmacodynamic marker in early drug development. Psychopharmacology (Berl) 2012; 220: 97-107.
82. Ebert U, Siepmann M, Oertel R, Wesnes KA, Kirch W. Pharmacokinetics and pharmacodynamics of scopolamine after subcutaneous administration. J Clin Pharmacol 1998; 38: 720-726.
83. Young JW, Powell SB, Geyer MA. Mouse pharmacological models of cognitive disruption relevant to schizophrenia. Neuropharmacology 2012; 62: 1381-1390.
84. Patel S, Tariot PN. Pharmacologic models of Alzheimer's disease. Psychiatr Clin North Am 1991; 14: 287-308.
85. Ebert U, Kirch W. Scopolamine model of dementia: electroencephalogram findings and cognitive performance. Eur J Clin Invest 1998; 28: 944-949.
86. Berardi AM, Parasuraman R, Haxby JV. Sustained attention in mild Alzheimer's disease. Dev Neuropsychol 2005; 28: 507-537.
87. Baddeley A, Cocchini G, Della Sala S, Logie RH, Spinnler H. Working memory and vigilance: evidence from normal aging and Alzheimer's disease. Brain Cogn 1999; 41: 87-108.
88. Gigout S, Jones GA, Wierschke S, Davies CH, Watson JM, Deisz RA. Distinct muscarinic acetylcholine receptor subtypes mediate pre- and postsynaptic effects in rat neocortex. BMC Neurosci 2012; 13: 42.
89. Klinkenberg I, Blokland A. The validity of scopolamine as a pharmacological model for cognitive impairment: a review of animal behavioral studies. Neurosci Biobehav Rev 2010; 34: 1307-1350.
90. McCool MF, Patel S, Talati R, Ragozzino ME. Differential involvement of M1-type and M4-type muscarinic cholinergic receptors in the dorsomedial striatum in task switching. Neurobiol Learn Mem 2008; 89: 114-124.
91. Harms LR, Turner KM, Eyles DW, Young JW, McGrath JJ, Burne TH. Attentional processing in C57BL/6J mice exposed to developmental vitamin D deficiency. PLoS One 2012; 7: e35896.
92. Bushnell PJ, Benignus VA, Case MW. Signal detection behavior in humans and rats: a comparison with matched tasks. Behavioral processes 2003; 64: 121-129.
93. Lennertz L, Wagner M, Frommann I, Schulze-Rauschenbach S, Schuhmacher A, Kuhn KU et al. A coding variant of the novel serotonin receptor subunit 5-HT3E influences sustained attention in schizophrenia patients. Eur Neuropsychopharmacol 2010; 20: 414-420.
94. Markov V, Krug A, Krach S, Jansen A, Eggermann T, Zerres K et al. Impact of schizophrenia-risk gene dysbindin 1 on brain activation in bilateral middle frontal gyrus during a working memory task in healthy individuals. Hum Brain Mapp 2010; 31: 266-275.
95. Neuhaus AH, Opgen-Rhein C, Urbanek C, Hahn E, Ta TM, Seidelsohn M et al. COMT Val 158 Met polymorphism is associated with cognitive flexibility in a signal discrimination task in schizophrenia. Pharmacopsychiatry 2009; 42: 141-144.
96. Eyler LT, Dawes SE, Asgaard GL, Young JW. Abnormalities of brain responses during vigilance and inhibition in bipolar disorder. Bipolar Disord 2011; 13(Suppl 1): 42.
97. McKenna B, Young JW, Dawes SE, Asgaard GL, Eyler LT. Bridging the bench to bedside gap: validation of a reverse-translated rodent continuous performance test using functional magnetic resonance imaging. Psychiatry Res 2013; 212: 183-191.
98. Young JW, Goey AK, Minassian A, Perry W, Paulus MP, Geyer MA. 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.
99. Young JW, van Enkhuizen J, Winstanley CA, Geyer MA. Increased risk-taking behavior in dopamine transporter knockdown mice: further support for a mouse model of mania. J Psychopharmacol 2011; 25: 934-943.