Eye Movement Dysfunction as a Biological Marker of Risk for Schizophrenia

Australian and New Zealand Journal of Psychiatry

Volumn 34, Issue , 2000, Pages S91-S100

  Lee, Kwang Hyuk ^a   Williams, Leanne M ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

genetics; high risk; saccade; schizophrenia; smooth pursuit eye movement (SPEM)

Indexed keywords

EYE MOVEMENT DISORDER; GENETIC MARKER; GENETICS; HUMAN; PHENOTYPE; PSYCHOLOGY; REVIEW; RISK FACTOR; SACCADIC EYE MOVEMENT; SCHIZOPHRENIA; SMOOTH PURSUIT EYE MOVEMENT;

GENETIC MARKERS; HUMANS; OCULAR MOTILITY DISORDERS; PHENOTYPE; PURSUIT, SMOOTH; RISK FACTORS; SACCADES; SCHIZOPHRENIA; SCHIZOPHRENIC PSYCHOLOGY;

EID: 0034320317     PISSN: 00048674     EISSN: 14401614     Source Type: Journal    
DOI: 10.1080/000486700228     Document Type: Article

References (116)

1. Holzman PS, Proctor LR, Hughes DW. Eye-tracking patterns in schizophrenia. Science 1973; 181:179-181.
2. Holzman PS, Proctor LR, Levy DL, Yasillo NJ, Meltzer HY, Hurt SW. Eye-tracking dysfunctions in schizophrenic patients and their relatives. Archives of General Psychiatry 1974; 31:143-151.
3. Levy DL, Holzman PS, Matthysse S, Mendell NR. Eye tracking dysfunction and schizophrenia: a critical perspective. Schizophrenia Bulletin 1993; 19:461-536.
4. Iacono WG, Peloquin LJ, Lumry AE, Valentine RH, Tuason VB. Eye tracking in patients with unipolar and bipolar affective disorders in remission. Journal of Abnormal Psychology 1982; 91:35-44.
5. Levy DL, Dorus E, Shaughnessy R et al. Pharmacologic evidence for specificity of pursuit dysfunction to schizophrenia. Lithium carbonate associated with abnormal pursuit. Archives of General Psychiatry 1985; 42:335-341.
6. Siever LJ, van Kammen DP, Linnoila M, Alterman I, Hare T, Murphy DL. Smooth pursuit eye movement disorder and its psychobiologic correlates in unmedicated schizophrenics. Biological Psychiatry 1986; 21:1167-1174.
7. Spohn HE, Coyne L, Spray J. The effect of neuroleptics and tardive dyskinesia on smooth-pursuit eye movement in chronic schizophrenics. Archives of General Psychiatry 1988; 45:833-840.
8. Siever LJ, Coursey RD, Alterman IS, Buchsbaum MS, Murphy DL. Impaired smooth pursuit eye movement: vulnerability marker for schizotypal personality disorder in a normal volunteer population. American Journal of Psychiatry 1984; 141:1560-1566.
9. Siever LJ, Friedman L, Moskowitz J et al. Eye movement impairment and schizotypal psychopathology. American Journal of Psychiatry 1994; 151:1209-1215.
10. Campion D, Thibaut F, Denise P, Courtin P, Pottier M, Levillain D. SPEM impairment in drug-naive schizophrenic patients: evidence for a trait marker. Biological Psychiatry 1992; 32:891-902.
11. Gooding DC, Iacono WG, Beiser M. Temporal stability of smooth-pursuit eye tracking in first-episode psychosis. Psychophysiology 1994; 31:62-67.
12. Yee CM, Nuechterlein KH, Dawson ME. A longitudinal analysis of eye tracking dysfunction and attention in recentonset schizophrenia. Psychophysiology 1998; 35:443-451.
13. Clementz BA, Sweeney JA. Is eye movement dysfunction a biological marker for schizophrenia? A methodological review. Psychological Bulletin 1990; 108:77-92.
14. Keefe RS, Silverman JM, Mohs RC et al. Eye tracking, attention, and schizotypal symptoms in nonpsychotic relatives of patients with schizophrenia. Archives of General Psychiatry 1997; 54:169-176.
15. Ross DE, Thaker GK, Buchanan RW, Lahti AC, Conley R, Medoff D. Specific measures account for most of the variance in qualitative ratings of smooth pursuit eye movements in schizophrenia. Archives of General Psychiatry 1998; 55:184-186.
16. Levin S, Luebke A, Zee DS, Hain TC, Robinson DA, Holzman PS. Smooth pursuit eye movements in schizophrenics: quantitative measurements with the searchcoil technique. Journal of Psychiatric Research 1988; 22:195-206.
17. Sweeney JA, Clementz BA, Haas GL, Escobar MD, Drake K, Frances AJ. Eye tracking dysfunction in schizophrenia: characterization of component eye movement abnormalities, diagnostic specificity, and the role of attention. Journal of Abnormal Psychology 1994; 103:222-230.
18. Sweeney JA, Luna B, Srinivasagam NM et al. Eye tracking abnormalities in schizophrenia: evidence for dysfunction in the frontal eye fields. Biological Psychiatry 1998; 44:698-708.
19. Hommer DW, Clem T, Litman R, Pickar D. Maladaptive anticipatory saccades in schizophrenia. Biological Psychiatry 1991; 30:779-794.
20. Litman RE, Hommer DW, Radant A, Clem T, Pickar D. Quantitative effects of typical and atypical neuroleptics on smooth pursuit eye tracking in schizophrenia. Schizophrenia Research 1994; 12:107-120.
21. Ross RG, Olincy A, Harris JG, Radant A, Adler LE, Freedman R. Anticipatory saccades during smooth pursuit eye movements and familial transmission of schizophrenia. Biological Psychiatry 1998; 44:690-697.
22. Flechtner KM, Steinacher B, Sauer R, Mackert A. Smooth pursuit eye movements in schizophrenia and affective disorder. Psychological Medicine 1997; 27:1411-1419.
23. Gaymard B, Pierrot-Deseilligny C. Neurology of saccades and smooth pursuit. Current Opinion in Neurology 1999; 12:13-19.
24. Sharpe JA. Cortical control of eye movements. Current Opinion in Neurology 1998; 11:31-38.
25. O'Driscoll GA, Strakowski SM, Alpert NM et al. Differences in cerebral activation during smooth pursuit and saccadic eye movements using positron-emission tomography. Biological Psychiatry 1998; 44:685-689.
26. Levin S. Frontal lobe dysfunctions in schizophrenia - I. Eye movement impairments. Journal of Psychiatric Research 1984; 18:27-55.
27. Katsanis J, Iacono W. Clinical, neuropsychological, and brain structural correlates of smooth-pursuit eye tracking performance in chronic schizophrenia. Journal of Abnormal Psychology 1991; 100:526-534.
28. Snitz BE, Curtis CE, Zald DH, Katsanis J, Iacono WG. Neuropsychological and oculomotor correlates of spatial working memory performance in schizophrenia patients and controls. Schizophrenia Research 1999; 38:37-50.
29. Nakashima Y, Momose T, Sano I et al. Cortical control of saccade in normal and schizophrenic subjects: a PET study using a task-evoked rCBF paradigm. Schizophrenia Research 1994; 12:259-264.
30. Ross DE, Thaker GK, Holcomb HH, Cascella NG, Medoff DR, Tamminga CA. Abnormal smooth pursuit eye movements in schizophrenic patients are associated with cerebral glucose metabolism in oculomotor regions. Psychiatry Research 1995; 58:53-67.
31. Thurston SE, Leigh RJ, Crawford T, Thompson A, Kennard C. Two distinct deficits of visual tracking caused by unilateral lesions of cerebral cortex in humans. Annals of Neurology 1988; 23:266-273.
32. Morrow MJ, Sharpe JA. Retinotopic and directional deficits of smooth pursuit initiation after posterior cerebral hemispheric lesions. Neurology 1993; 43:595-603.
33. Clementz BA. Saccades to moving targets in schizophrenia: Evidence for normal posterior cortex functioning. Psychophysiology 1996; 33:650-654.
34. Chen Y, Levy DL, Nakayama K, Matthysse S, Palafox G, Holzman P.S. Dependence of impaired eye tracking on deficient velocity discrimination in schizophrenia. Archives of General Psychiatry 1999; 56:155-161.
35. Holzman PS. Eye movements and the search for the essence of schizophrenia. Brain Research Reviews 2000; 31:350-356.
36. MacAvoy MG, Bruce CJ. Comparison of the smooth eye tracking disorder of schizophrenics with that of nonhuman primates with specific brain lesions. International Journal of Neuroscience 1995; 80:117-151.
37. Trillenberg P, Heide W, Junghanns K, Blankenburg M, Arolt V, Kompf D. Target anticipation and impairment of smooth pursuit eye movements in schizophrenia. Experimental Brain Research 1998; 120:316-324.
38. Fukushima J, Fukushima K, Chiba T, Tanaka S, Yamashita I, Kato M. Disturbances of voluntary control of saccadic eye movements in schizophrenic patients. Biological Psychiatry 1988; 23:670-677.
39. Fukushima J, Morita N, Fukushima K, Chiba T, Tanaka S, Yamashita I. Voluntary control of saccadic eye movements in patients with schizophrenic and affective disorders. Journal of Psychiatric Research 1990; 24:9-24.
40. Clementz BA, McDowell JE, Zisook S. Saccadic system functioning among schizophrenia patients and their first-degree biological relatives. Journal of Abnormal Psychology 1994; 103:277-287.
41. Nieman DH, Bour LJ, Linszen DH et al. Neuropsychological and clinical correlates of antisaccade task performance in schizophrenia. Neurology 2000; 54:866-871.
42. Karoumi B, Ventre-Dominey J, Vighetto A, Dalery J, d'Amato T. Saccadic eye movements in schizophrenic patients. Psychiatry Research 1998; 77:9-19.
43. Radant AD, Claypoole K, Wingerson DK, Cowley DS, Roy-Byrne PP. Relationships between neuropsychological and oculomotor measures in schizophrenia patients and normal controls. Biological Psychiatry 1997; 42:797-805.
44. Rosse RB, Schwartz BL, Kim SY, Deutsch SI. Correlation between antisaccade and Wisconsin Card Sorting Test performance in schizophrenia. American Journal of Psychiatry 1993; 150:333-335.
45. Tien AY, Ross DE, Pearlson G, Strauss ME. Eye movements and psychopathology in schizophrenia and bipolar disorder. Journal of Nervous and Mental Disease 1996; 184:331-338.
46. Guitton D, Buchtel HA, Douglas RM. Frontal lobe lesions in man cause difficulties in suppressing reflexive glances and in generating goal-directed saccades. Experimental Brain Research 1985; 58:455-472.
47. Walker R, Husain M, Hodgson TL, Harrison J, Kennard C. Saccadic eye movement and working memory deficits following damage to human prefrontal cortex. Neuropsychologia 1998; 36:1141-1159.
48. O'Driscoll GA, Alpert NM, Matthysse SW, Levy DL, Rauch SL, Holzman PS. Functional neuroanatomy of antisaccade eye movements investigated with positron emission tomography. Proceedings of the National Academy of Sciences of the USA 1995; 92:925-929.
49. Muri RM, Heid O, Nirkko AC et al. Functional organisation of saccades and antisaccades in the frontal lobe in humans: a study with echo planar functional magnetic resonance imaging. Journal of Neurology, Neurosurgery and Psychiatry 1998; 65:374-377.
50. Everling S, Fischer B. The antisaccade: a review of basic research and clinical studies. Neuropsychologia 1998; 36:885-899.
51. Cassady SL, Thaker GK, Tamminga CA. Pharmacologic relationship of antisaccade and dyskinesia in schizophrenic patients. Psychopharmacology Bulletin 1993; 29:235-240.
52. Fischer B, Weber H, Biscaldi M, Aiple F, Otto P, Stuhr V. Separate populations of visually guided saccades in humans: reaction times and amplitudes. Experimental Brain Research 1993; 92:528-541.
53. Schiller PH, Sandell JH, Maunsell JH. The effect of frontal eye field and superior colliculus lesions on saccadic latencies in the rhesus monkey. Journal of Neurophysiology 1987; 57:1033-1049.
54. Munoz DP, Wurtz RH. Role of the rostral superior colliculus in active visual fixation and execution of express saccades. Journal of Neurophysiology 1992; 67:1000-1002.
55. Sommer MA. Express saccades elicited during visual scan in the monkey. Vision Research 1994; 34:2023-2038.
56. Sommer MA. The spatial relationship between scanning saccades and express saccades. Vision Research 1997; 37:2745-2756.
57. Clementz BA. The ability to produce express saccades as a function of gap interval among schizophrenia patients. Experimental Brain Research 1996; 111:121-130.
58. Matsue Y, Osakabe K, Saito H et al. Smooth pursuit eye movements and express saccades in schizophrenic patients. Schizophrenia Research 1994; 12:121-130.
59. Sereno AB, Holzman PS. Express saccades and smooth pursuit eye movement function in schizophrenic, affective disorder, and normal subjects. Journal of Cognitive Neuroscience 1993; 5:303-316.
60. Mialet JP, Pichot P. Eye-tracking patterns in schizophrenia. An analysis based on the incidence of saccades. Archives of General Psychiatry 1981; 38:183-186.
61. Matsue Y, Okuma T, Saito H et al. Saccadic eye movements in tracking, fixation, and rest in schizophrenic and normal subjects. Biological Psychiatry 1986; 21:382-389.
62. Fischer B, Weber H. Saccadic reaction times of dyslexic and age-matched normal subjects. Perception 1990; 19:805-818.
63. Braun D, Weber H, Mergner T, Schulte-Monting J. Saccadic reaction times in patients with frontal and parietal lesions. Brain 1992; 115:1359-1386.
64. Matsue Y, Saito H, Osakabe K et al. Smooth pursuit eye movements and voluntary control of saccades in the antisaccade task in schizophrenic patients. Japanese Journal of Psychiatry and Neurology 1994; 48:13-22.
65. Sereno AB, Holzman PS. Antisaccades and smooth pursuit eye movements in schizophrenia. Biological Psychiatry 1995; 37:394-401.
66. Holzman PS, Solomon CM, Levin S, Waternaux CS. Pursuit eye movement dysfunctions in schizophrenia. Family evidence for specificity. Archives of General Psychiatry 1984; 41:136-139.
67. Iacono WG, Moreau M, Beiser M, Fleming JA, Lin TY. Smooth-pursuit eye tracking in first-episode psychotic patients and their relatives. Journal of Abnormal Psychology 1992; 101:104-116.
68. Levy DL, Yasillo NJ, Dorus E et al. Relatives of unipolar and bipolar patients have normal pursuit. Psychiatry Research 1983; 10:285-293.
69. Green MF. Schizophrenia from a neurocognitive perspective. Needham Heights, MA: Allyn and Bacon, 1998.
70. Kinney DK, Levy DL, Yurgelun-Todd DA, Lajonchere CM, Holzman PS. Eye-tracking dysfunction and birth-month weather in schizophrenia. Journal of Abnormal Psychology 1999; 108:359-362.
71. Kinney DK, Levy DL, Yurgelun-Todd DA, Tramer SJ, Holzman PS. Inverse relationship of perinatal complications and eye tracking dysfunction in relatives of patients with schizophrenia: evidence for a two-factor model. American Journal of Psychiatry 1998; 155:976-978.
72. Mather JA. Eye movements of teenage children of schizophrenics: a possible inherited marker of susceptibility to the disease. Journal of Psychiatric Research 1985; 19:523-532.
73. Schwartz BD, O'Brien BA, Evans WJ, Sautter FJ Jr, Winstead DK. Smooth pursuit eye movement differences between familial and non-familial schizophrenia. Schizophrenia Research 1995; 17:211-219.
74. Thaker GK, Cassady S, Adami H, Moran M, Ross DE. Eye movements in spectrum personality disorders: comparison of community subjects and relatives of schizophrenic patients. American Journal of Psychiatry 1996; 153:362-368.
75. Clementz BA, Sweeney JA, Hirt M, Haas G. Pursuit gain and saccadic intrusions in first-degree relatives of probands with schizophrenia. Journal of Abnormal Psychology 1990; 99:327-335.
76. Iacono WG, Lykken DT. Eye tracking and psychopathology. New procedures applied to a sample of normal monozygotic twins. Archives of General Psychiatry 1979; 36:1361-1369.
77. Holzman PS, Kringlen E, Matthysse S et al. A single dominant gene can account for eye tracking dysfunctions and schizophrenia in offspring of discordant twins. Archives of General Psychiatry 1988; 45:641-647.
78. Grove WM, Clementz BA, Iacono WG, Katsanis J. Smooth pursuit ocular motor dysfunction in schizophrenia: evidence for a major gene. American Journal of Psychiatry 1992; 149:1362-1368.
79. Grove WM, Iacono WG. Comment on Levy et al. Eye tracking dysfunction and schizophrenia. Schizophrenia Bulletin 1994; 20:781-786.
80. Grove WM, Lebow BS, Clementz BA, Cerri A, Medus C, Iacono WG. Familial prevalence and coaggregation of schizotypy indicators: a multitrait family study. Journal of Abnormal Psychology 1991; 100:115-121.
81. Ross RG, Harris JG, Olincy A, Radant A, Adler LE, Freedman R. Familial transmission of two independent saccadic abnormalities in schizophrenia. Schizophrenia Research 1998; 30:59-70.
82. Rosenberg DR, Sweeney JA, Squires-Wheeler E, Keshavan MS, Cornblatt BA, Erlenmeyer-Kimling L. Eye-tracking dysfunction in offspring from the New York High-Risk Project: diagnostic specificity and the role of attention. Psychiatry Research 1997; 66:121-130.
83. McDowell JE, Myles-Worsley M, Coon H, Byerley W, Clementz BA. Measuring liability for schizophrenia using optimized antisaccade stimulus parameters. Psychophysiology 1999; 36:138-141.
84. Crawford TJ, Sharma T, Puri BK, Murray RM, Berridge DM, Lewis SW. Saccadic eye movements in families multiply affected with schizophrenia: the Maudsley Family Study. American Journal of Psychiatry 1998; 155:1703-1710.
85. Holzman PS, Coleman M, Lenzenweger MF et al. Working memory deficits, antisaccades, and thought disorder in relation to perceptual aberration. In: Raine A, Lencz T, Mednick SA, eds. Schizotypal Personality. Cambridge, Cambridge University Press, 1995:353-381.
86. Lencz T, Raine A, Scerbo A et al. Impaired eye tracking in undergraduates with schizotypal personality disorder. American Journal of Psychiatry 1993; 150:152-154.
87. Siever LJ, Coursey RD, Alterman IS et al. Clinical, psychophysiological, and neurological characteristics of volunteers with impaired smooth pursuit eye movements. Biological Psychiatry 1989; 26:35-51.
88. Coursey RD, Lees RW, Siever LJ. The relationship between smooth pursuit eye movement impairment and psychological measures of psychopathology. Psychological Medicine 1989; 19:343-358.
89. Simons RF, Katkin W. Smooth pursuit eye movements in subjects reporting physical anhedonia and perceptual aberrations. Psychiatry Research 1985; 14:275-289.
90. Gooding DC, Miller MD, Kwapil TR. Smooth pursuit eye tracking and visual fixation in psychosis-prone individuals. Psychiatry Research 2000; 93:41-54.
91. O'Driscoll GA, Lenzenweger MF, Holzman PS. Antisaccades and smooth pursuit eye tracking and schizotypy. Archives of General Psychiatry 1998; 55: 837-843.
92. Thaker G, Moran M, Cassady S, Adami H, Tamminga C. Normal smooth pursuit eye movements in volunteer subjects meeting schizotypal personality disorder criteria. American Journal of Psychiatry 1991; 148:1096-1097.
93. Malaspina D, Friedman JH, Kaufmann C et al. Psychobiological heterogeneity of familial and sporadic schizophrenia. Biological Psychiatry 1998; 43:489-496.
94. Litman RE, Torrey EF, Hommer DW, Radant AR, Pickar D, Weinberger DR. A quantitative analysis of smooth pursuit eye tracking in monozygotic twins discordant for schizophrenia. Archives of General Psychiatry 1997; 54: 417-426.
95. Ross RG, Radant AD, Hommer DW. A developmental study of smooth pursuit eye movements in normal children from 7 to 15 years of age. Journal of the American Academy of Child and Adolescent Psychiatry 1993; 32:783-791.
96. Ross RG, Olincy A, Harris JG et al. The effects of age on a smooth pursuit tracking task in adults with schizophrenia and normal subjects. Biological Psychiatry 1999; 46:383-391.
97. Spooner JW, Sakala SM, Baloh RW. Effect of aging on eye tracking. Archives of Neurology 1980; 37:575-576.
98. Jacobsen LK, Hong WL, Hommer DW et al. Smooth pursuit eye movements in childhood-onset schizophrenia: comparison with attention-deficit hyperactivity disorder and normal controls. Biological Psychiatry 1996; 40:1144-1154.
99. Ross RG, Hommer D, Radant A, Roath M, Freedman R. Early expression of smooth-pursuit eye movement abnormalities in children of schizophrenic parents. Journal of the American Academy of Child and Adolescent Psychiatry 1996; 35:941-949.
100. Fischer B, Biscaldi M, Gezeck S. On the development of voluntary and reflexive components in human saccade generation. Brain Research 1997; 754:285-297.
101. Weinberger DR. Implications of normal brain development for the pathogenesis of schizophrenia. Archives of General Psychiatry 1987; 44:660-669.
102. Olincy A, Ross RG, Youngd DA, Freedman R. Age diminishes performance on an antisaccade eye movement task. Neurobiology of Aging 1997; 18:483-489.
103. Schlenker R, Cohen R. Smooth-pursuit eye-movement dysfunction and motor control in schizophrenia: a follow-up study. European Archives of Psychiatry and Clinical Neuroscience 1995; 245:125-126.
104. Hutton S, Kennard C. Oculomotor abnormalities in schizophrenia: a critical review. Neurology 1998; 50:604-609.
105. Kelly P, Rennie C, Gordon E, Anderson J, Howson A, Meares R. Smooth pursuit eye tracking dysfunction and negative symptoms in schizophrenia. Psychiatry Research 1990; 34:89-97.
106. Gaebel W, Ulrich G. Visuomotor tracking performance in schizophrenia: relationship with psychopathological subtyping. Neuropsychobiology 1987; 17:66-71.
107. Solomon CM, Holzman PS, Levin S, Gale HJ. The association between eye-tracking dysfunctions and thought disorder in psychosis. Archives of General Psychiatry 1987; 44:31-35.
108. Liddle PF. The symptoms of chronic schizophrenia. A re-examination of the positive-negative dichotomy. British Journal of Psychiatry 1987; 151:145-151.
109. Lee K-H, Williams LM, Loughland CM, Davidson D. Smooth-pursuit eye movement dysfunction and syndromes in schizophrenia. Australian Psychiatric Research Annual Scientific Meeting, 2-3 December, Sydney, Australia, 1999.
110. Arndt S, Andreasen NC, Miller D, Nopoulos P. A longitudinal study of symptom dimensions in schizophrenia: prediction and patterns of change. Archives of General Psychiatry 1995; 52:353-360.
111. Cardno AG, Holmans PA, Harvey I, Williams MB, Owen MJ, McGuffin P. Factor-derived subsyndromes of schizophrenia and familial morbid risks. Schizophrenia Research 1997; 23:231-238.
112. Loftus J, DeLisi LE, Crow TJ. Familial associations of subsyndromes of psychosis in affected sibling pairs with schizophrenia and schizoaffective disorder. Psychiatry Research 1998; 80:101-111.
113. Serretti A, Macciardi F, Smeraldi E. Dopamine receptor D2 Ser/Cys311 variant associated with disorganized symptomatology of schizophrenia. Schizophrenia Research 1998; 34:207-210.
114. Gaebel W, Ulrich G, Frick K. Visuomotor performance of schizophrenic patients and normal controls in a picture viewing task. Biological Psychiatry 1987; 22:1227-1237.
115. Gordon E, Coyle S, Anderson J et al. Eye movement response to a facial stimulus in schizophrenia. Biological Psychiatry 1992; 31:626-629.
116. Williams LM, Loughland CM, Gordon E, Davidson D. Visual scanpaths in schizophrenia: is there a deficit in face recognition? Schizophrenia Research 1999; 40:189-199.