Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-23T11:01:36.708Z Has data issue: false hasContentIssue false
  • English
  • Français

Integrated assessment of visual perception abnormalities in psychotic disorders and relationship with clinical characteristics

Published online by Cambridge University Press:  04 September 2018

Halide Bilge Türközer ,
Tuna Hasoğlu ,
Yue Chen ,
Lesley Anne Norris ,
Meredith Brown ,
Nathaniel Delaney-Busch ,
Emre H. Kale ,
Zahide Pamir ,
Hüseyin Boyacı  and
Gina Kuperberg
...Show all authors
Halide Bilge Türközer
Affiliation:
McLean Hospital, Belmont, and Harvard Medical School, Boston, MA, USA Department of Psychiatry, The University of Texas Southwestern Medical Center, Dallas, TX, USA Department of Psychiatry, Marmara University School of Medicine, Istanbul, Turkey
Tuna Hasoğlu
Affiliation:
McLean Hospital, Belmont, and Harvard Medical School, Boston, MA, USA
Yue Chen
Affiliation:
McLean Hospital, Belmont, and Harvard Medical School, Boston, MA, USA
Lesley Anne Norris
Affiliation:
McLean Hospital, Belmont, and Harvard Medical School, Boston, MA, USA
Meredith Brown
Affiliation:
Department of Psychology, Tufts University, Medford, MA, USA Department of Psychiatry, Massachusetts General Hospital, Boston, MA, USA
Nathaniel Delaney-Busch
Affiliation:
Department of Psychology, Tufts University, Medford, MA, USA
Emre H. Kale
Affiliation:
Brain Research Center, Ankara University, Ankara, Turkey
Zahide Pamir
Affiliation:
Neuroscience Graduate Program, Bilkent University, Ankara, Turkey
Hüseyin Boyacı
Affiliation:
Neuroscience Graduate Program, Bilkent University, Ankara, Turkey Department of Psychology, Bilkent University, Ankara, Turkey Department of Psychology, JL Giessen University, Giessen, Germany
Gina Kuperberg
Affiliation:
Department of Psychology, Tufts University, Medford, MA, USA Department of Psychiatry, Massachusetts General Hospital, Boston, MA, USA
Kathryn E. Lewandowski
Affiliation:
McLean Hospital, Belmont, and Harvard Medical School, Boston, MA, USA
Volkan Topçuoğlu
Affiliation:
Department of Psychiatry, Marmara University School of Medicine, Istanbul, Turkey
Dost Öngür*
Affiliation:
McLean Hospital, Belmont, and Harvard Medical School, Boston, MA, USA
*
Author for correspondence: Dost Öngür, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

The visual system is recognized as an important site of pathology and dysfunction in schizophrenia. In this study, we evaluated different visual perceptual functions in patients with psychotic disorders using a potentially clinically applicable task battery and assessed their relationship with symptom severity in patients, and with schizotypal features in healthy participants.

Methods

Five different areas of visual functioning were evaluated in patients with schizophrenia and schizoaffective disorder (n = 28) and healthy control subjects (n = 31) using a battery that included visuospatial working memory (VSWM), velocity discrimination (VD), contour integration, visual context processing, and backward masking tasks.

Results

The patient group demonstrated significantly lower performance in VD, contour integration, and VSWM tasks. Performance did not differ between the two groups on the visual context processing task and did not differ across levels of interstimulus intervals in the backward masking task. Performances on VSWM, VD, and contour integration tasks were correlated with negative symptom severity but not with other symptom dimensions in the patient group. VSWM and VD performances were also correlated with negative sychizotypal features in healthy controls.

Conclusion

Taken together, these results demonstrate significant abnormalities in multiple visual processing tasks in patients with psychotic disorders, adding to the literature implicating visual abnormalities in these conditions. Furthermore, our results show that visual processing impairments are associated with the negative symptom dimension in patients as well as healthy individuals.

Keywords

Context processingcontour integrationpsychosisschizophreniavelocity discriminationvisuospatial working memory
Type
Original Articles
Information
Psychological Medicine , Volume 49 , Issue 10 , July 2019 , pp. 1740 - 1748
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alloway, TP (2007) Automated Working Memory Assessment. London: Pearson Assessment.Google Scholar
Altmann, CF, Bülthoff, HH and Kourtzi, Z (2003) Perceptual organization of local elements into global shapes in the human visual cortex. Current Biology 13, 342–349.10.1016/S0960-9822(03)00052-6Google Scholar
American Psychiatric Association (2000) Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition, Text Review. Washington, DC: American Psychiatric Press.Google Scholar
Anderson, EJ, Tibber, MS, Schwarzkopf, DS, Shergill, SS, Fernandez-Egea, E, Rees, G and Dakin, SC (2017) Visual population receptive fields in people with schizophrenia have reduced inhibitory surrounds. The Journal of Neuroscience 37, 1546–1556.Google Scholar
Bartel, P, Blom, M, Robinson, E, Van Der Meyden, C, De Sommers, K and Becker, P (1990) The effects of levodopa and haloperidol on flash and pattern ERGs and VEPs in normal humans. Documenta Ophthalmologica 76, 55–64.10.1007/BF00140498Google Scholar
Bressan, P and Kramer, P (2013) The relation between cognitive-perceptual schizotypal traits and the Ebbinghaus size-illusion is mediated by judgment time. Frontiers in Psychology 4, 343.Google Scholar
Brugger, SP and Howes, OD (2017) Heterogeneity and homogeneity of regional brain structure in schizophrenia: a meta-analysis. JAMA Psychiatry 74, 1104–1111.Google Scholar
Butler, PD, Martinez, A, Foxe, JJ, Kim, D, Zemon, V, Silipo, G, Mahoney, J, Shpaner, M, Jalbrzikowski, M and Javitt, DC (2007) Subcortical visual dysfunction in schizophrenia drives secondary cortical impairments. Brain 130, 417–430.Google Scholar
Butler, PD, Abeles, IY, Silverstein, SM, Dias, EC, Weiskopf, NG, Calderone, DJ and Sehatpour, P (2013) An event-related potential examination of contour integration deficits in schizophrenia. Frontiers in Psychology 4, 1–12.Google Scholar
Cappe, C, Herzog, MH, Herzig, DA, Brand, A and Mohr, C (2012) Cognitive disorganisation in schizotypy is associated with deterioration in visual backward masking. Psychiatry Research 200, 652–659.10.1016/j.psychres.2012.07.001Google Scholar
Carter, C, Robertson, L, Nordahl, T, Chaderjian, M, Kraft, L and O'Shora-Celaya, L (1996) Spatial working memory deficits and their relationship to negative symptoms in unmedicated schizophrenia patients. Biological Psychiatry 40, 930–932.10.1016/S0006-3223(96)00350-2Google Scholar
Chen, Y, Nakayama, K, Levy, DL, Matthysse, S and Holzman, PS (1999 a) Psychophysical isolation of a motion-processing deficit in schizophrenics and their relatives and its association with impaired smooth pursuit. Proceedings of the National Academy of Sciences of the USA 96, 4724–4729.10.1073/pnas.96.8.4724Google Scholar
Chen, Y, Palafox, GP, Nakayama, K, Levy, DL, Matthysse, S and Holzman, PS (1999 b) Motion perception in schizophrenia. Archives of General Psychiatry 56, 149–154.Google Scholar
Chen, Y, Bidwell, LC and Holzman, PS (2005) Visual motion integration in schizophrenia patients, their first-degree relatives, and patients with bipolar disorder. Schizophrenia Research 74, 271–281.10.1016/j.schres.2004.04.002Google Scholar
Chen, Y, Levy, DL, Sheremata, S and Holzman, PS (2006) Bipolar and schizophrenic patients differ in patterns of visual motion discrimination. Schizophrenia Research 88, 208–216.10.1016/j.schres.2006.06.004Google Scholar
Coleman, MJ, Cook, S, Matthysse, S, Barnard, J, Lo, Y, Levy, DL, Rubin, DB and Holzman, PS (2002) Spatial and object working memory impairments in schizophrenia patients: a Bayesian item-response theory analysis. Journal of Abnormal Psychology 111, 425–435.Google Scholar
Dakin, S, Carlin, P and Hemsley, D (2005) Weak suppression of visual context in chronic schizophrenia. Current Biology 15, 822–824.10.1016/j.cub.2005.10.015Google Scholar
Fang, F, Boyaci, H, Kersten, D and Murray, SO (2008) Attention-dependent representation of a size illusion in human V1. Current Biology 18, 1707–1712.Google Scholar
First, MB, Spitzer, RL, Gibbon, M and Williams, JB (2002) Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition (SCID-I/P). New York, NY: Biometrics Research, New York State Psychiatric Institute.Google Scholar
Fonseca-Pedrero, E, Badoud, D, Antico, L, Caputo, GB, Eliez, S, Schwartz, S and Debbané, M (2015) Strange-face-in-the-mirror illusion and schizotypy during adolescence. Schizophrenia Bulletin 41, 475–482.10.1093/schbul/sbu196Google Scholar
van der Gaag, M, Hoffman, T, Remijsen, M, Hijman, R, de Haan, L, van Meijel, B, van Harten, PN, Valmaggia, L, de Hert, M, Cuijpers, A and Wiersma, D (2006) The five-factor model of the Positive and Negative Syndrome Scale II: A ten-fold cross-validation of a revised model. Schizophrenia Research 85, 280–287.10.1016/j.schres.2006.03.021Google Scholar
Garcia-Portilla, MP, Garcia-Alvarez, L, Saiz, PA, Al-Halabi, S, Bobes-Bascaran, MT, Bascaran, MT, Muñiz, J and Bobes, J (2015) Psychometric evaluation of the negative syndrome of schizophrenia. European Archives of Psychiatry and Clinical Neuroscience 265, 559–566.Google Scholar
Gooding, DC and Tallent, KA (2003) Spatial, object, and affective working memory in social anhedonia: an exploratory study. Schizophrenia Research 63, 247–260.10.1016/S0920-9964(02)00326-2Google Scholar
Green, MF, Nuechterlein, KH and Mintz, J (1994) Backward masking in schizophrenia and mania: I. specifying a mechanism. Archives of General Psychiatry 51, 939–944.10.1001/archpsyc.1994.03950120011003Google Scholar
Green, MF, Nuechterlein, KH, Breitmeyer, B and Mintz, J (2006) Forward and backward visual masking in unaffected siblings of schizophrenic patients. Biological Psychiatry 59, 446–451.10.1016/j.biopsych.2005.06.035Google Scholar
Hollingshead, A (1975) Four Factor Index of Social Status. New Haven, CT: Yale University.Google Scholar
Horton, HK and Silverstein, SM (2011) Visual context processing deficits in schizophrenia: effects of deafness and disorganization. Schizophrenia Bulletin 37, 716–726.Google Scholar
Hutchinson, CV, Walker, JA and Davidson, C (2014) Oestrogen, ocular function and low-level vision: a review. The Journal of Endocrinology 223, R9–18.Google Scholar
Iuvone, PM, Tigges, M, Fernandes, A and Tigges, J (1989) Dopamine synthesis and metabolism in rhesus monkey retina: development, aging, and the effects of monocular visual deprivation. Visual Neuroscience 2, 465–471.10.1017/S0952523800012360Google Scholar
Joseph, J, Bae, G and Silverstein, SM (2013) Sex, symptom, and premorbid social functioning associated with perceptual organization dysfunction in schizophrenia. Frontiers in Psychology 4, 1–9.Google Scholar
Kantrowitz, JT, Butler, PD, Schecter, I, Silipo, G and Javitt, DC (2009) Seeing the world dimly: the impact of early visual deficits on visual experience in schizophrenia. Schizophrenia Bulletin 35, 1085–1094.Google Scholar
Kay, SR, Fiszbein, A and Opler, LA (1987) The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261–276.Google Scholar
Kent, BW, Weinstein, ZA, Passarelli, V, Chen, Y and Siever, LJ (2011) Deficient visual sensitivity in schizotypal personality disorder. Schizophrenia Research 127, 144–150.Google Scholar
Kéri, S, Kiss, I, Kelemen, O, Benedek, G and Janka, Z (2005) Anomalous visual experiences, negative symptoms, perceptual organization and the magnocellular pathway in schizophrenia: a shared construct? Psychological Medicine 35, 1445–1455.Google Scholar
Kim, D, Wylie, G, Pasternak, R, Butler, P and Javitt, DC (2006) Magnocellular contributions to impaired motion processing in schizophrenia. Schizophrenia Research 82, 1–8.Google Scholar
Klosterkotter, J, Hellmich, M, Steinmeyer, EM and Schultze-Lutter, F (2001) Diagnosing schizophrenia in the initial prodromal phase. Archives of General Psychiatry 58, 158–164.10.1001/archpsyc.58.2.158Google Scholar
Koethe, D, Kranaster, L, Hoyer, C, Gross, S, Neatby, MA, Schultze-Lutter, F, Ruhrmann, S, Klosterkötter, J, Hellmich, M and Leweke, FM (2009) Binocular depth inversion as a paradigm of reduced visual information processing in prodromal state, antipsychotic-naïve and treated schizophrenia. European Archives of Psychiatry and Clinical Neuroscience 259, 195–202.10.1007/s00406-008-0851-6Google Scholar
Kourtzi, Z, Tolias, AS, Altmann, CF, Augath, M and Logothetis, NK (2003) Integration of local features into global shapes: monkey and human fMRI studies. Neuron 37, 333–346.Google Scholar
Lee, J and Park, S (2005) Working memory impairments in schizophrenia: a meta-analysis. Journal of Abnormal Psychology 114, 599–611.Google Scholar
Leiderman, EA and Strejilevich, SA (2004) Visuospatial deficits in schizophrenia: central executive and memory subsystems impairments. Schizophrenia Research 68, 217–223.Google Scholar
Levitt, H (1971) Transformed up- down methods in psychoacoustics. Journal of the Acoustics Society of America 49, 467–477.Google Scholar
Martinez, A, Hillyard, SA, Dias, EC, Hagler, DJ Jr, Butler, PD, Guilfoyle, DN, Jalbrzikowski, M, Silipo, G and Javitt, DC (2008) Magnocellular pathway impairment in schizophrenia: evidence from functional magnetic resonance imaging. Journal of Neuroscience 28, 7492–7500.10.1523/JNEUROSCI.1852-08.2008Google Scholar
McMains, SA and Kastner, S (2010) Defining the units of competition: influences of perceptual organization on competitive interactions in human visual cortex. Journal of Cognitive Neuroscience 22, 2417–2426.10.1162/jocn.2009.21391Google Scholar
Mittal, VA, Gupta, T, Keane, BP and Silverstein, SM (2015) Visual context processing dysfunctions in youth at high risk for psychosis: resistance to the Ebbinghaus illusion and its symptom and social and role functioning correlates. Journal of Abnormal Psychology 124, 953–960.Google Scholar
Owoso, A, Carter, CS, Gold, JM, MacDonald, AW, Ragland, JD, Silverstein, SM, Strauss, ME and Barch, DM (2013) Cognition in schizophrenia and schizo-affective disorder: impairments that are more similar than different. Psychological Medicine 43, 2535–2545.10.1017/S0033291713000536Google Scholar
Pantelis, C, Stuart, GW, Nelson, HE, Robbins, TW and Barnes, TRE (2001) Spatial working memory deficits in schizophrenia: relationship with tardive dyskinesia and negative symptoms. American Journal of Psychiatry 158, 1276–1285.Google Scholar
Park, S and Gooding, DC (2014) Working memory impairment as an endophenotypic marker of a schizophrenia diathesis. Schizophrenia Research: Cognition 1, 127–136.Google Scholar
Park, S and McTigue, K (1997) Working memory and syndromes of schizotypal personality. Schizophrenia Research 26, 213–220.10.1016/S0920-9964(97)00051-0Google Scholar
Park, S, Holzman, PS and Lenzenweger, MF (1995) Individual differences in spatial working memory in relation to schizotypy. Journal of Abnormal Psychology 104, 355–363.Google Scholar
Park, S, Püschel, J, Sauter, BH, Rentsch, M and Hell, D (1999) Spatial working memory deficits and clinical symptoms in schizophrenia: a 4-month follow-up study. Biological Psychiatry 46, 392–400.Google Scholar
Pawełczyk, A, Kotlicka-Antczak, M, Rabe-Jabłońska, J, Pawełczyk, T, Ruszpel, A and Łojek, E (2015) Figural fluency and immediate visual memory in patients with at-risk mental state for psychosis: empirical study. Early Intervention in Psychiatry 9, 324–330.10.1111/eip.12116Google Scholar
Perossini, M and Fornaro, P (1990) Electroretinographic effects induced in humans by psychopharmacologic agents. Documenta Ophthalmologica 75, 1–6.Google Scholar
Raine, A (1991) The SPQ: a scale for the assessment of schizotypal personality based on DSM-III-R criteria. Schizophrenia Bulletin 17, 555–564.10.1093/schbul/17.4.555Google Scholar
Ribolsi, M, Lisi, G, Di Lorenzo, G, Rociola, G, Niolu, C and Siracusano, A (2013) Negative correlation between leftward bias in line bisection and schizotypal features in healthy subjects. Frontiers in Psychology 4, 846.Google Scholar
Schubert, EW, Henriksson, KM and McNeil, TF (2005) A prospective study of offspring of women with psychosis: visual dysfunction in early childhood predicts schizophrenia-spectrum disorders in adulthood. Acta Psychiatrica Scandinavica 112, 385–393.Google Scholar
Sheffield, JM, Gold, JM, Strauss, ME, Carter, CS, MacDonald, AW, Ragland, JD, Silverstein, SM and Barch, DM (2014) Common and specific cognitive deficits in schizophrenia: relationships to function. Cognitive, Affective, & Behavioral Neuroscience 14, 161–174.Google Scholar
Silverstein, SM (2016) Visual perception disturbances in schizophrenia: a unified model. In Li, M and Spaulding, WD (eds), The Neuropsychopathology of Schizophrenia. Switzerland: Springer International Publishing, pp. 77–132.Google Scholar
Silverstein, SM and Keane, BP (2011 a) Perceptual organization impairment in schizophrenia and associated brain mechanisms: review of research from 2005 to 2010. Schizophrenia Bulletin 37, 690–699.Google Scholar
Silverstein, SM and Keane, BP (2011 b) Vision science and schizophrenia research: toward a re-view of the disorder editors’ introduction to special section. Schizophrenia Bulletin 37, 681–689.Google Scholar
Silverstein, S, Uhlhaas, PJ, Essex, B, Halpin, S, Schall, U and Carr, V (2006) Perceptual organization in first episode schizophrenia and ultra-high-risk states. Schizophrenia Research 83, 41–52.Google Scholar
Silverstein, SM, Berten, S, Essex, B, Kovács, I, Susmaras, T and Little, DM (2009) An fMRI examination of visual integration in schizophrenia. Journal of Integrative Neuroscience 8, 175–202.Google Scholar
Silverstein, SM, Keane, BP, Barch, DM, Carter, CS, Gold, JM, Kovács, I, MacDonald, A, Ragland, JD and Strauss, ME (2012) Optimization and validation of a visual integration test for schizophrenia research. Schizophrenia Bulletin 38, 125–134.Google Scholar
Silverstein, SM, Harms, MP, Carter, CS, Gold, JM, Keane, BP, MacDonald, A, Daniel Ragland, J and Barch, DM (2015) Cortical contributions to impaired contour integration in schizophrenia. Neuropsychologia 75, 469–480.Google Scholar
Tadin, D, Kim, J, Doop, ML, Gibson, C, Lappin, JS, Blake, R and Park, S (2006) Weakened center-surround interactions in visual motion processing in schizophrenia. Journal of Neuroscience 26, 11403–11412.Google Scholar
Tallent, KA and Gooding, DC (1999) Working memory and Wisconsin Card Sorting Test performance in schizotypic individuals: a replication and extension. Psychiatry Research 89, 161–170.Google Scholar
Tamminga, CA, Ivleva, EI, Keshavan, MS, Pearlson, GD, Clementz, BA, Witte, B, Morris, DW, Bishop, J, Thaker, GK and Sweeney, JA (2013) Clinical Phenotypes of psychosis in the Bipolar-Schizophrenia Network on Intermediate Phenotypes (B-SNIP). American Journal of Psychiatry 170, 1263–1274.10.1176/appi.ajp.2013.12101339Google Scholar
Uhlhaas, PJ, Silverstein, SM, Phillips, WA and Lovell, PG (2004) Evidence for impaired visual context processing in schizotypy with thought disorder. Schizophrenia Research 68, 249–260.Google Scholar
Uhlhaas, PJ, Phillips, WA and Silverstein, SM (2005) The course and clinical correlates of dysfunctions in visual perceptual organization in schizophrenia during the remission of psychotic symptoms. Schizophrenia Research 75, 183–192.Google Scholar
Uhlhaas, PJ, Phillips, WA, Mitchell, G and Silverstein, SM (2006 a) Perceptual grouping in disorganized schizophrenia. Psychiatry Research 145, 105–117.Google Scholar
Uhlhaas, PJ, Phillips, WA, Schenkel, LS and Silverstein, SM (2006 b) Theory of mind and perceptual context-processing in schizophrenia. Cognitive Neuropsychiatry 11, 416–436.Google Scholar
Ungerleider, L and Haxby, JV (1994) ‘What’ and ‘where’ in the human brain. Current Opinion in Neurobiology 4, 157–165.Google Scholar
Ungerleider, LG, Courtney, SM and Haxby, JV (1998) A neural system for human visual working memory. Proceedings of the National Academy of Sciences of the USA 95, 883–890.Google Scholar
Yang, E, Tadin, D, Glasser, DM, Hong, SW, Blake, R and Park, S (2013) Visual context processing in schizophrenia. Clinical Psychological Science 1, 5–15.10.1177/2167702612464618Google Scholar
Yoon, JH, Sheremata, SL, Rokem, A and Silver, MA (2013) Windows to the soul: vision science as a tool for studying biological mechanisms of information processing deficits in schizophrenia. Frontiers in Psychology 4, 1–15.Google Scholar
Ziermans, TB (2013) Working memory capacity and psychotic-like experiences in a general population sample of adolescents and young adults. Frontiers in Psychiatry 4, 161.10.3389/fpsyt.2013.00161Google Scholar
Supplementary material: File

Türközer et al. supplementary material

Türközer et al. supplementary material 1

Download Türközer et al. supplementary material(File)
File 168 KB