Simple viewing tests can detect eye movement abnormalities that distinguish schizophrenia cases from controls with exceptional accuracy

Biological Psychiatry

Volumn 72, Issue 9, 2012, Pages 716-724

  Benson, Philip J ^a   Beedie, Sara A ^a   Shephard, Elizabeth ^a   Giegling, Ina ^b   Rujescu, Dan ^b   St Clair, David ^a,c  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b UNIVERSITY OF MUNICH   (Germany)

^c NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

Classification; eye movement phenotype; neural network; predictive model; risk marker; schizophrenia

Indexed keywords

NEUROLEPTIC AGENT;

ACCURACY; ADULT; ARTICLE; CONTROLLED STUDY; EYE MOVEMENT DISORDER; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MALE; PREDICTIVE VALIDITY; PRIORITY JOURNAL; SCHIZOPHRENIA; SMOKING; SMOOTH PURSUIT EYE MOVEMENT; STRUCTURED CLINICAL INTERVIEW FOR DSM DISORDERS;

ADULT; CASE-CONTROL STUDIES; EYE MOVEMENTS; FEMALE; HUMANS; MALE; MODELS, STATISTICAL; NEUROPSYCHOLOGICAL TESTS; OCULAR MOTILITY DISORDERS; PREDICTIVE VALUE OF TESTS; SCHIZOPHRENIA; SMOKING; TIME FACTORS;

EID: 84867088878     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2012.04.019     Document Type: Article

References (58)

1. A.R. Diefendorf, R. Dodge An experimental study of the ocular reactions of the insane from photographic records Brain 31 1908 451 489
2. P.S. Holzman, L.R. Proctor, D.L. Levy, N.J. Yasillo, H.Y. Meltzer, S.W. Hurt Eye-tracking dysfunctions in schizophrenic patients and their relatives Arch Gen Psychiatry 31 1974 143 151
3. D.L. Levy, R.B. Lipton, P.S. Holzman, J.M. Davis Eye tracking dysfunction unrelated to clinical state and treatment with haloperidol Biol Psychiatry 18 1983 813 819
4. P.S. Holzman, C.M. Solomon, S. Levin, C.S. Waternaux Pursuit eye movement dysfunctions in schizophrenia Family evidence for specificity Arch Gen Psychiatry 41 1984 136 139
5. D.H. Blackwood, D.M. St. Clair, W.J. Muir, J.C. Duffy Auditory P300 and eye tracking dysfunction in schizophrenic pedigrees Arch Gen Psychiatry 48 1991 899 909
6. B.A. Clementz, W.M. Grove, W.G. Iacono, J.A. Sweeney Smooth-pursuit eye movement dysfunction and liability for schizophrenia: Implications for genetic modeling J Abnorm Psychol 101 1992 117 129
7. W.M. Grove, B.A. Clementz, W.G. Iacono, J. Katsanis Smooth pursuit ocular motor dysfunction in schizophrenia: Evidence for a major gene Am J Psychiatry 149 1992 1362 1368
8. W.G. Iacono, M. Moreau, M. Beiser, J.A. Fleming, T.Y. Lin Smooth-pursuit eye tracking in first-episode psychotic patients and their relatives J Abnorm Psychol 101 1992 104 116
9. D.E. Ross, G.K. Thaker, R.W. Buchanan, A.C. Lahti, D. Medoff, J.J. Bartko Association of abnormal smooth pursuit eye movements with the deficit syndrome in schizophrenic patients Am J Psychiatry 153 1996 1158 1165
10. R.E. Litman, E.F. Torrey, D.W. Hommer, A.R. Radant, D. Pickar, D.R. Weinberger A quantitative analysis of smooth pursuit eye tracking in monozygotic twins discordant for schizophrenia Arch Gen Psychiatry 54 1997 417 426
11. B. Karoumi, M. Saoud, T. d'Amato, F. Rosenfeld, P. Denise, C. Gutknecht Poor performance in smooth pursuit and antisaccadic eye-movement tasks in healthy siblings of patients with schizophrenia Psychiatry Res 101 2001 209 219
12. J.K. Rybakowski, A. Borkowska Eye movement and neuropsychological studies in first-degree relatives of schizophrenic patients Schizophr Res 54 2002 105 110
13. U. Ettinger, V. Kumari, T.J. Crawford, P.J. Corr, M. Das, E. Zachariah Smooth pursuit and antisaccade eye movements in siblings discordant for schizophrenia J Psychiatr Res 38 2004 177 184
14. L.E. Hong, B.D. Mitchell, M.T. Avila, H. Adami, R.P. McMahon, G.K. Thaker Familial aggregation of eye-tracking endophenotypes in families of schizophrenic patients Arch Gen Psychiatry 63 2006 259 264
15. M.J. van Tricht, D.H. Nieman, L.J. Bour, T. Boeree, J.H. Koelman, L. de Haan Increased saccadic rate during smooth pursuit eye movements in patients at ultra high risk for developing a psychosis Brain Cogn 73 2010 215 221
16. J.S. Allen, K. Matsunaga, T. Nakamura, F. Kitamura, T. Furukawa, S.S. Hacisalihzade Schizophrenia, eye movements, and biocultural heterogeneity Hum Biol 62 1990 337 352
17. D. Campion, F. Thibaut, P. Denise, P. Courtin, M. Pottier, D. Levillain SPEM impairment in drug-naive schizophrenic patients: Evidence for a trait marker Biol Psychiatry 32 1992 891 902
18. S. Louchart-de la Chapelle, I. Nkam, E. Houy, A. Belmont, J.F. Menard, A.C. Roussignol A concordance study of three electrophysiological measures in schizophrenia Am J Psychiatry 162 2005 466 474
19. R. Lencer, K. Trillenberg-Krecker, E. Schwinger, V. Arolt Schizophrenia spectrum disorders and eye tracking dysfunction in singleton and multiplex schizophrenia families Schizophr Res 60 2003 33 45
20. X.F. Amador, H.A. Sackeim, S. Mukherjee, R. Halperin, P. Neeley, E. Maclin Specificity of smooth pursuit eye movement and visual fixation abnormalities in schizophrenia Comparison to mania and normal controls Schizophr Res 5 1991 135 144
21. D.C. Gooding, J.A. Grabowski, C.S. Hendershot Fixation stability in schizophrenia, bipolar, and control subjects Psychiatry Res 97 2000 119 128
22. J.J. Barton, M. Pandita, K. Thakkar, D.C. Goff, D.S. Manoach The relation between antisaccade errors, fixation stability and prosaccade errors in schizophrenia Exp Brain Res 186 2008 273 282
23. H.M. Haraldsson, U. Ettinger, B.B. Magnusdottir, T. Sigmundsson, E. Sigurdsson, H. Petursson Eye movement deficits in schizophrenia: Investigation of a genetically homogenous Icelandic sample Eur Arch Psychiatry Clin Neurosci 258 2008 373 383
24. X.F. Amador, D. Malaspina, H.A. Sackeim, E.A. Coleman, C.A. Kaufmann, A. Hasan Visual fixation and smooth pursuit eye movement abnormalities in patients with schizophrenia and their relatives J Neuropsychiatry Clin Neurosci 7 1995 197 206
25. J. Kissler, B.A. Clementz Fixation stability among schizophrenia patients Neuropsychobiology 38 1998 57 62
26. Y. Hori, H. Fukuzako, Y. Sugimoto, M. Takigawa Eye movements during the Rorschach test in schizophrenia Psychiatry Clin Neurosci 56 2002 409 418
27. M.J. Green, J.H. Waldron, I. Simpson, M. Coltheart Visual processing of social context during mental state perception in schizophrenia J Psychiatry Neurosci 33 2008 34 42
28. M.L. Phillips, A.S. David Visual scan paths are abnormal in deluded schizophrenics Neuropsychologia 35 1997 99 105
29. B.R. Manor, E. Gordon, L.M. Williams, C.J. Rennie, H. Bahramali, C.R. Latimer Eye movements reflect impaired face processing in patients with schizophrenia Biol Psychiatry 46 1999 963 969
30. C.M. Loughland, L.M. Williams, E. Gordon Visual scanpaths to positive and negative facial emotions in an outpatient schizophrenia sample Schizophr Res 55 2002 159 170
31. T. Kojima, E. Matsushima, K. Nakajima, H. Shiraishi, K. Ando, H. Ando Eye movements in acute, chronic, and remitted schizophrenics Biol Psychiatry 27 1990 975 989
32. T. Kojima, E. Matsushima, K. Ohta, M. Toru, Y.H. Han, Y.C. Shen Stability of exploratory eye movements as a marker of schizophrenia - a WHO multi-center study World Health Organization Schizophr Res 52 2001 203 213
33. P.E. Bestelmeyer, B.W. Tatler, L.H. Phillips, G. Fraser, P.J. Benson, D. St. Clair Global visual scanning abnormalities in schizophrenia and bipolar disorder Schizophr Res 87 2006 212 222
34. P.J. Benson, U. Leonards, R.M. Lothian, D.M. St Clair, M.C. Merlo Visual scan paths in first-episode schizophrenia and cannabis-induced psychosis J Psychiatry Neurosci 32 2007 267 274
35. M.L. Xia, S. Takahashi, E. Tanabe, M. Matsuura, T. Kojima, E. Matsushima Eye movement studies on schizophrenics and their parents Eur Neuropsychopharmacol 6 1 1996 64-64
36. C.M. Loughland, L.M. Williams, A.W. Harris Visual scanpath dysfunction in first-degree relatives of schizophrenia probands: Evidence for a vulnerability marker? Schizophr Res 67 2004 11 21
37. S. Takahashi, E. Tanabe, K. Yara, M. Matsuura, E. Matsushima, T. Kojima Impairment of exploratory eye movement in schizophrenia patients and their siblings Psychiatry Clin Neurosci 62 2008 487 493
38. M. Takahashi, H. Hayashi, Y. Watanabe, K. Sawamura, N. Fukui, J. Watanabe Diagnostic classification of schizophrenia by neural network analysis of blood-based gene expression signatures Schizophr Res 119 2010 210 218
39. M.B. First, R.L. Spitzer, M. Gibbon, J.B.W. Williams Structured Clinical Interview for DSM-IV Axis I Disorders - Patient Edition (SCID I/P, Version 2.0) 1997 New York State Psychiatric Institute, Biometrics Research Department New York
40. P. McGuffin, A. Farmer, I. Harvey A polydiagnostic application of operational criteria in studies of psychotic illness: Development and reliability of the OPCRIT system Arch Gen Psychiatry 48 1991 764 770
41. C. Ambroise, G.J. McLachlan Selection bias in gene extraction on the basis of microarray gene-expression data Proc Natl Acad Sci U S A 99 2002 6562 6566
42. W.J. Muir, D.M. St. Clair, D.H. Blackwood, H.M. Roxburgh, I. Marshall Eye-tracking dysfunction in the affective psychoses and schizophrenia Psychol Med 22 1992 573 580
43. B. Efron, R.J. Tibshirani An Introduction to the Bootstrap 1993 Chapman and Hall/CRC Boca Raton, FL
44. W.J. Conover, R.L. Iman Rank transformations as a bridge between parametric and nonparametric statistics Am Statistician 35 1981 124 129
45. J. Cohen Statistical Power Analysis for the Behavioral Sciences 2nd ed. 1988 Lawrence Erlbaum Associates Mahwah, NJ
46. W. Venables Calculation of confidence intervals for noncentrality parameters J Roy Stat Soc B 37 1975 406 412
47. L.V. Hedges, I. Olkin Statistical Methods for Meta-Analysis 1985 Academic Press Orlando, FL
48. W.L. Hays Statistics for Psychologists 1963 Holt, Rinehart and Winston New York
49. G. Keppel Design and Analysis: A Researcher's Handbook 1991 Prentice Hall Englewood Cliffs, NJ
50. Gideon Schwarz Estimating the dimension of a model Ann Statist 6 1978 461 464
51. L. Breiman, J. Friedman, C.J. Stone, R.A. Olshen Classification and Regression Trees 1984 Wadsworth & Brooks/Cole Advanced Books & Software Monterey, CA
52. J.H. Friedman Greedy function approximation: A gradient boosting machine Ann Statistics 29 2001 1189 1232
53. J.H. Friedman Stochastic gradient boosting Comput Stat Data Anal 38 2002 367 378
54. Caruana R, Niculescu-Mizil A (2006): An empirical comparison of supervised learning algorithms. Proceedings of the 23rd International Conference on Machine Learning; Carnegie Mellon University, Pittsburgh, Pennsylvania; 25-29 Jun. 148:161-168.
55. D.F. Specht Probabilistic neural networks and the polynomial Adaline as complementary techniques for classification IEEE Trans Neural Netw 1 1990 111 121
56. D.F. Specht Enhancements to probabilistic neural networks Neural Netw 1 1992 761 768
57. A.M. Molinaro, R. Simon, R.M. Pfeiffer Prediction error estimation: A comparison of resampling methods Bioinformatics 21 2005 3301 3307
58. F. Bono, R.L. Oliveri, M. Zappia, U. Aguglia, G. Puccio, A. Quattrone Computerized analysis of eye movements as a function of age Arch Gerontol Geriatr 22 1996 261