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Reduced influence of perceptual context in schizophrenia: behavioral and neurophysiological evidence

Published online by Cambridge University Press:  20 December 2019

Victor J. Pokorny Open the ORCID record for Victor J. Pokorny [Opens in a new window] ,
Timothy J. Lano ,
Michael-Paul Schallmo Open the ORCID record for Michael-Paul Schallmo [Opens in a new window] ,
Cheryl A. Olman Open the ORCID record for Cheryl A. Olman [Opens in a new window]  and
Scott R. Sponheim
Victor J. Pokorny
Affiliation:
Minneapolis Veterans Affairs Health Care System, Minneapolis, MN55417, USA
Timothy J. Lano
Affiliation:
Minneapolis Veterans Affairs Health Care System, Minneapolis, MN55417, USA Department of Psychiatry and Behavioral Science, University of Minnesota, Minneapolis, MN, USA
Michael-Paul Schallmo
Affiliation:
Department of Psychiatry and Behavioral Science, University of Minnesota, Minneapolis, MN, USA
Cheryl A. Olman
Affiliation:
Department of Psychology, University of Minnesota, Minneapolis, MN, USA
Scott R. Sponheim*
Affiliation:
Minneapolis Veterans Affairs Health Care System, Minneapolis, MN55417, USA Department of Psychiatry and Behavioral Science, University of Minnesota, Minneapolis, MN, USA
*
Author for correspondence: Scott R. Sponheim, E-mail: [email protected]
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Abstract

Background

Accurate perception of visual contours is essential for seeing and differentiating objects in the environment. Both the ability to detect visual contours and the influence of perceptual context created by surrounding stimuli are diminished in people with schizophrenia (SCZ). The central aim of the present study was to better understand the biological underpinnings of impaired contour integration and weakened effects of perceptual context. Additionally, we sought to determine whether visual perceptual abnormalities reflect genetic factors in SCZ and are present in other severe mental disorders.

Methods

We examined behavioral data and event-related potentials (ERPs) collected during the perception of simple linear contours embedded in similar background stimuli in 27 patients with SCZ, 23 patients with bipolar disorder (BP), 23 first-degree relatives of SCZ, and 37 controls.

Results

SCZ exhibited impaired visual contour detection while BP exhibited intermediate performance. The orientation of neighboring stimuli (i.e. flankers) relative to the contour modulated perception across all groups, but SCZ exhibited weakened suppression by the perceptual context created by flankers. Late visual (occipital P2) and cognitive (centroparietal P3) neural responses showed group differences and flanker orientation effects, unlike earlier ERPs (occipital P1 and N1). Moreover, behavioral effects of flanker context on contour perception were correlated with modulation in P2 & P3 amplitudes.

Conclusion

In addition to replicating and extending findings of abnormal contour integration and visual context modulation in SCZ, we provide novel evidence that the abnormal use of perceptual context is associated with higher-order sensory and cognitive processes.

Keywords

ContextcontourEEGperceptionpsychosisschizophrenia
Type
Original Article
Information
Psychological Medicine , Volume 51 , Issue 5 , April 2021 , pp. 786 - 794
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Copyright
Copyright © Cambridge University Press 2019

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References

American Psychological Association (2000). Diagnostic and statistical manual of mental disorders (Vol. 75, 4th ed., pp. 78–85, Text Revision). Washington, DC: American Psychiatric Association.Google Scholar
Angelucci, A., & Bressloff, P. C. (2006). Contribution of feedforward, lateral and feedback connections to the classical receptive field center and extra-classical receptive field surround of primate V1 neurons. In Martinez-Conde, S., Macknik, S. L., Martinez, L. M., Alonso, J.-M., & Tse, P. U. (Eds.), Progress in Brain Research (Vol. 154, pp. 93–120). Amsterdam, Netherlands: Elsevier. https://doi.org/10.1016/S0079-6123(06)54005-1.Google Scholar
Bair, W., Cavanaugh, J. R., & Movshon, J. A. (2003). Time course and time-distance relationships for surround suppression in macaque V1 neurons. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 23(20), 7690–7701. https://doi.org/10.1523/JNEUROSCI.23-20-07690.2003.CrossRefGoogle ScholarPubMed
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B, Statistical Methodology, 57(1), 289–300. Retrieved from http://www.jstor.org/stable/2346101.Google Scholar
Bledowski, C., Prvulovic, D., Hoechstetter, K., Scherg, M., Wibral, M., Goebel, R., & Linden, D. E. J.(2004). Localizing P300 generators in visual target and distractor processing: A combined event-related potential and functional magnetic resonance imaging study. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 24(42), 9353–9360. https://doi.org/10.1523/JNEUROSCI.1897-04.2004.CrossRefGoogle ScholarPubMed
Bramon, E., McDonald, C., Croft, R. J., Landau, S., Filbey, F., Gruzelier, J. H., … Murray, R. M. (2005). Is the P300 wave an endophenotype for schizophrenia? A meta-analysis and a family study. NeuroImage, 27(4), 960–968. https://doi.org/10.1016/j.neuroimage.2005.05.022.CrossRefGoogle Scholar
Butler, P. D., Abeles, I. Y., Silverstein, S. M., Dias, E. C., Weiskopf, N. G., Calderone, D. J., & Sehatpour, P.(2013). An event-related potential examination of contour integration deficits in schizophrenia. Frontiers in Psychology, 4, 132. https://doi.org/10.3389/fpsyg.2013.00132.CrossRefGoogle Scholar
Cai, Y., Zhou, T., & Chen, L. (2008). Effects of binocular suppression on surround suppression. Journal of Vision, 8(9), 9.1–910. https://doi.org/10.1167/8.9.9.CrossRefGoogle ScholarPubMed
Chubb, C., Sperling, G., & Solomon, J. A. (1989). Texture interactions determine perceived contrast. Proceedings of the National Academy of Sciences of the United States of America, 86(23), 9631–9635. https://doi.org/10.1073/pnas.86.23.9631.CrossRefGoogle ScholarPubMed
Dakin, S., Carlin, P., & Hemsley, D. (2005). Weak suppression of visual context in chronic schizophrenia. Current Biology: CB, 15(20), R822–R824. https://doi.org/10.1016/j.cub.2005.10.015.CrossRefGoogle ScholarPubMed
Dakin, S. C., & Baruch, N. J. (2009). Context influences contour integration. Journal of Vision, 9(2), 13.1–13.13. https://doi.org/10.1167/9.2.13.CrossRefGoogle ScholarPubMed
Donchin, E., & Coles, M. G. H. (1988). Is the P300 component a manifestation of context updating? The Behavioral and Brain Sciences, 11(3), 357–374. https://doi.org/10.1017/S0140525X00058027.CrossRefGoogle Scholar
Feng, Q., Zheng, Y., Zhang, X., Song, Y., Luo, Y.-J., Li, Y., & Talhelm, T. (2011). Gender differences in visual reflexive attention shifting: Evidence from an ERP study. Brain Research, 1401, 59–65. https://doi.org/10.1016/j.brainres.2011.05.041.CrossRefGoogle ScholarPubMed
First, M. B., Spitzer, R. L., Gibbon, M., & Williams, J. B. W. (2002). Structured clinical interview for DSM-IV-TR axis I disorders, research version, patient edition. New York, NY: SCID-I/P.Google Scholar
Foxe, J. J., Murray, M. M., & Javitt, D. C. (2005). Filling-in in schizophrenia: A high-density electrical mapping and source-analysis investigation of illusory contour processing. Cerebral Cortex, 15(12), 1914–1927. https://doi.org/10.1093/cercor/bhi069.CrossRefGoogle ScholarPubMed
Garcia-Perez, M. A. (2000). Optimal setups for forced-choice staircases with fixed step sizes. Spatial Vision, 13(4), 431–448. Retrieved from http://www.springerlink.com/index/R045N3P44UT407Q4.pdf.CrossRefGoogle ScholarPubMed
Goghari, V. M., Macdonald, A. W. III, & Sponheim, S. R. (2014). Relationship between prefrontal gray matter volumes and working memory performance in schizophrenia: A family study. Schizophrenia Research, 153(1–3), 113–121. https://doi.org/10.1016/j.schres.2014.01.032.CrossRefGoogle ScholarPubMed
Gold, J. M., & Dickinson, D. (2013). [Review of “Generalized Cognitive Deficit” In schizophrenia: Overused Or underappreciated?]. Schizophrenia Bulletin, 39(2), 263–265. https://doi.org/10.1093/schbul/sbs143.CrossRefGoogle Scholar
Hetrick, W. P., Erickson, M. A., & Smith, D. A. (2012). Phenomenological dimensions of sensory gating. Schizophrenia Bulletin, 38(1), 178–191. https://doi.org/10.1093/schbul/sbq054.CrossRefGoogle ScholarPubMed
Jeon, Y.-W., & Polich, J. (2003). Meta-analysis of P300 and schizophrenia: Patients, paradigms, and practical implications. Psychophysiology, 40(5), 684–701. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/14696723.CrossRefGoogle ScholarPubMed
Johannesen, J. K., O'Donnell, B. F., Shekhar, A., McGrew, J. H., & Hetrick, W. P. (2013). Diagnostic specificity of neurophysiological endophenotypes in schizophrenia and bipolar disorder. Schizophrenia Bulletin, 39(6), 1219–1229. https://doi.org/10.1093/schbul/sbs093.CrossRefGoogle ScholarPubMed
Johnson, R. Jr (1986). A triarchic model of P300 amplitude. Psychophysiology, 23(4), 367–384. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/3774922.CrossRefGoogle ScholarPubMed
Keane, B. P., Joseph, J., & Silverstein, S. M. (2014). Late, not early, stages of Kanizsa shape perception are compromised in schizophrenia. Neuropsychologia, 56, 302–311. https://doi.org/10.1016/j.neuropsychologia.2014.02.001.CrossRefGoogle ScholarPubMed
Kelly, S. P., & O'Connell, R. G. (2013). Internal and external influences on the rate of sensory evidence accumulation in the human brain. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 33(50), 19434–19441. https://doi.org/10.1523/JNEUROSCI.3355-13.2013.CrossRefGoogle ScholarPubMed
Luck, S. J., Kappenman, E. S., Fuller, R. L., Robinson, B., Summerfelt, A., & Gold, J. M. (2009). Impaired response selection in schizophrenia: Evidence from the P3 wave and the lateralized readiness potential. Psychophysiology, 46(4), 776–786. https://doi.org/10.1111/j.1469-8986.2009.00817.x.CrossRefGoogle ScholarPubMed
Lynn, P. A., Kang, S. S., & Sponheim, S. R. (2016). Impaired retrieval processes evident during visual working memory in schizophrenia. Schizophrenia Research: Cognition, 5, 47. https://doi.org/10.1016/j.scog.2016.07.002.Google Scholar
Maekawa, T., Katsuki, S., Kishimoto, J., Onitsuka, T., Ogata, K., Yamasaki, T., … Kanba, S. (2013). Altered visual information processing systems in bipolar disorder: Evidence from visual MMN and P3. Frontiers in Human Neuroscience, 7, 403. https://doi.org/10.3389/fnhum.2013.00403.CrossRefGoogle ScholarPubMed
Mittal, V. A., Gupta, T., Keane, B. P., & Silverstein, S. M. (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(4), 953–960. https://doi.org/10.1037/abn0000082.CrossRefGoogle ScholarPubMed
Morey, R. D. (2008). Confidence intervals from normalized data: A correction to Cousineau (2005). Tutorials in Quantitative Methods for Psychology, 4(2), 61–64. https://doi.org/10.20982/tqmp.04.2.p061.CrossRefGoogle Scholar
Nurminen, L., Merlin, S., Bijanzadeh, M., Federer, F., & Angelucci, A. (2018). Top-down feedback controls spatial summation and response amplitude in primate visual cortex. Nature Communications, 9(1), 2281. https://doi.org/10.1038/s41467-018-04500-5.CrossRefGoogle ScholarPubMed
O'Connell, R. G., Dockree, P. M., & Kelly, S. P. (2012). A supramodal accumulation-to-bound signal that determines perceptual decisions in humans. Nature Neuroscience, 15(12), 1729–1735. https://doi.org/10.1038/nn.3248.CrossRefGoogle ScholarPubMed
Overall, J. E., & Gorham, D. R. (1962). The brief psychiatric rating scale. Psychological Reports, 10(3), 799–812. https://doi.org/10.2466/pr0.1962.10.3.799.CrossRefGoogle Scholar
Petrov, Y., & McKee, S. P. (2009). The time course of contrast masking reveals two distinct mechanisms of human surround suppression. Journal of Vision, 9(1), 21.1–21.11. https://doi.org/10.1167/9.1.21.CrossRefGoogle ScholarPubMed
Portin, R., Kovala, T., Polo-Kantola, P., Revonsuo, A., Müller, K., & Matikainen, E. (2000). Does P3 reflect attentional or memory performances, or cognition more generally? Scandinavian Journal of Psychology, 41(1), 31–40. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/10731841.CrossRefGoogle ScholarPubMed
Raine, A. (1991). The SPQ: A scale for the assessment of schizotypal personality based on DSM-III-R criteria. Schizophrenia Bulletin, 17(4), 555–564. https://doi.org/10.1093/schbul/17.4.555.CrossRefGoogle ScholarPubMed
Ryu, V., An, S. K., Jo, H. H., & Cho, H. S. (2010). Decreased P3 amplitudes elicited by negative facial emotion in manic patients: Selective deficits in emotional processing. Neuroscience Letters, 481(2), 92–96. https://doi.org/10.1016/j.neulet.2010.06.059.CrossRefGoogle ScholarPubMed
Schallmo, M.-P., Kale, A. M., & Murray, S. O. (2019). The time course of different surround suppression mechanisms. Journal of Vision, 19(4), 12. https://doi.org/10.1167/19.4.12.CrossRefGoogle ScholarPubMed
Schallmo, M.-P., & Murray, S. O. (2016). Identifying separate components of surround suppression. Journal of Vision, 16(1), 2. https://doi.org/10.1167/16.1.2.CrossRefGoogle ScholarPubMed
Schallmo, M.-P., Sponheim, S. R., & Olman, C. A. (2013). Abnormal contextual modulation of visual contour detection in patients with schizophrenia. PLoS One, 8(6), e68090. https://doi.org/10.1371/journal.pone.0068090.CrossRefGoogle ScholarPubMed
Schallmo, M.-P., Sponheim, S. R., & Olman, C. A. (2015). Reduced contextual effects on visual contrast perception in schizophrenia and bipolar affective disorder. Psychological Medicine, 45(16), 3527–3537. https://doi.org/10.1017/S0033291715001439.CrossRefGoogle ScholarPubMed
Schumacher, J. F., Quinn, C. F., & Olman, C. A. (2011). An exploration of the spatial scale over which orientation-dependent surround effects affect contour detection. Journal of Vision, 11(8), 12. https://doi.org/10.1167/11.8.12.CrossRefGoogle ScholarPubMed
Silverstein, S. M., Harms, M. P., Carter, C. S., Gold, J. M., Keane, B. P., MacDonald, A. III, … Barch, D. M. (2015). Cortical contributions to impaired contour integration in schizophrenia. Neuropsychologia, 75, 469–480. https://doi.org/10.1016/j.neuropsychologia.2015.07.003.CrossRefGoogle Scholar
Silverstein, S. M., & Keane, B. P. (2011). Perceptual organization impairment in schizophrenia and associated brain mechanisms: Review of research from 2005 to 2010. Schizophrenia Bulletin, 37(4), 690–699. https://doi.org/10.1093/schbul/sbr052.CrossRefGoogle ScholarPubMed
Silverstein, S. M., Kovács, I., Corry, R., & Valone, C. (2000). Perceptual organization, the disorganization syndrome, and context processing in chronic schizophrenia. Schizophrenia Research, 43(1), 11–20. https://doi.org/10.1016/S0920-9964(99)00180-2.CrossRefGoogle ScholarPubMed
Snowden, R. J., & Hammett, S. T. (1998). The effects of surround contrast on contrast thresholds, perceived contrast and contrast discrimination. Vision Research, 38(13), 1935–1945. https://doi.org/10.1016/S0042-6989(97)00379-9.CrossRefGoogle ScholarPubMed
Spencer, K. M., Nestor, P. G., Niznikiewicz, M. A., Salisbury, D. F., Shenton, M. E., & McCarley, R. W. (2003). Abnormal neural synchrony in schizophrenia. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 23(19), 7407–7411. https://doi.org/10.1523/JNEUROSCI.23-19-07407.2003.CrossRefGoogle Scholar
Spencer, K. M., Nestor, P. G., Perlmutter, R., Niznikiewicz, M. A., Klump, M. C., Frumin, M., … McCarley, R. W. (2004). Neural synchrony indexes disordered perception and cognition in schizophrenia. Proceedings of the National Academy of Sciences of the United States of America, 101(49), 17288–17293. https://doi.org/10.1073/pnas.0406074101.CrossRefGoogle ScholarPubMed
Steffensen, S. C., Ohran, A. J., Shipp, D. N., Hales, K., Stobbs, S. H., & Fleming, D. E. (2008). Gender-selective effects of the P300 and N400 components of the visual evoked potential. Vision Research, 48(7), 917–925. https://doi.org/10.1016/j.visres.2008.01.005.CrossRefGoogle ScholarPubMed
Tagliabue, C. F., Veniero, D., Benwell, C. S. Y., Cecere, R., Savazzi, S., & Thut, G. (2019). The EEG signature of sensory evidence accumulation during decision formation closely tracks subjective perceptual experience. Scientific Reports, 9(1), 4949. https://doi.org/10.1038/s41598-019-41024-4.CrossRefGoogle ScholarPubMed
Tibber, M. S., Anderson, E. J., Bobin, T., Antonova, E., Seabright, A., Wright, B., … Dakin, S. C. (2013). Visual surround suppression in schizophrenia. Frontiers in Psychology, 4, 88. https://doi.org/10.3389/fpsyg.2013.00088.CrossRefGoogle Scholar
Twomey, D. M., Murphy, P. R., Kelly, S. P., & O'Connell, R. G. (2015). The classic P300 encodes a build-to-threshold decision variable. The European Journal of Neuroscience, 42(1), 1636–1643. https://doi.org/10.1111/ejn.12936.CrossRefGoogle ScholarPubMed
van der Stelt, O., Frye, J., Lieberman, J. A., & Belger, A. (2004). Impaired P3 generation reflects high-level and progressive neurocognitive dysfunction in schizophrenia. Archives of General Psychiatry, 61(3), 237–248. https://doi.org/10.1001/archpsyc.61.3.237.CrossRefGoogle Scholar
Webb, B. S., Dhruv, N. T., Solomon, S. G., Tailby, C., & Lennie, P. (2005). Early and late mechanisms of surround suppression in striate cortex of macaque. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 25(50), 11666–11675. https://doi.org/10.1523/JNEUROSCI.3414-05.2005.CrossRefGoogle ScholarPubMed
Wechsler, D. (1997). Manual for the Wechsler adult intelligence scale – third edition (WAIS-III). San Antonio, TX: The Psychological Corporation.Google Scholar
Wertheimer, M. (1938). Gestalt theory. In Ellis, W. D. (Ed.), A source book of Gestalt psychology (Vol. 403, pp. 1–11). London, England: Kegan Paul, Trench, Trubner & Company. https://doi.org/10.1037/11496-001.Google Scholar
Xing, J., & Heeger, D. J. (2000). Center-surround interactions in foveal and peripheral vision. Vision Research, 40(22), 3065–3072. https://doi.org/10.1016/S0042-6989(00)00152-8.CrossRefGoogle ScholarPubMed
Xing, J., & Heeger, D. J. (2001). Measurement and modeling of center-surround suppression and enhancement. Vision Research, 41(5), 571–583. https://doi.org/10.1016/S0042-6989(00)00270-4.CrossRefGoogle ScholarPubMed
Yang, E., Tadin, D., Glasser, D. M., Hong, S. W., Blake, R., & Park, S. (2013). Visual context processing in schizophrenia. Clinical Psychological Science, 1(1), 5–15. https://doi.org/10.1177/2167702612464618.CrossRefGoogle Scholar
Yoon, J. H., Rokem, A. S., Silver, M. A., Minzenberg, M. J., Ursu, S., Ragland, J. D., & Carter, C. S.(2009). Diminished orientation-specific surround suppression of visual processing in schizophrenia. Schizophrenia Bulletin, 35(6), 1078–1084. https://doi.org/10.1093/schbul/sbp064.CrossRefGoogle Scholar
Yu, C., Klein, S. A., & Levi, D. M. (2001). Surround modulation of perceived contrast and the role of brightness induction. Journal of Vision, 1(1), 18–31. https://doi.org/10.1167/1.1.3.CrossRefGoogle ScholarPubMed
Yu, C., Klein, S. A., & Levi, D. M. (2003). Cross- and iso-oriented surrounds modulate the contrast response function: The effect of surround contrast. Journal of Vision, 3(8), 527–540. https://doi.org/10.1167/3.8.1.CrossRefGoogle ScholarPubMed
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