Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-29T20:17:10.279Z Has data issue: false hasContentIssue false

Reduced contextual effects on visual contrast perception in schizophrenia and bipolar affective disorder

Published online by Cambridge University Press:  28 August 2015

M.-P. Schallmo*
Affiliation:
Graduate Program in Neuroscience, University of Minnesota, Minneapolis, MN, USA
S. R. Sponheim
Affiliation:
Veterans Affairs Medical Center, Minneapolis, MN, USA Department of Psychiatry, University of Minnesota, Minneapolis, MN, USA Department of Psychology, University of Minnesota, Minneapolis, MN, USA
C. A. Olman
Affiliation:
Department of Psychology, University of Minnesota, Minneapolis, MN, USA
*
* Address for correspondence: M.-P. Schallmo, Graduate Program in Neuroscience, University of Minnesota, Minneapolis, MN, USA. (Email: [email protected])

Abstract

Background.

The salience of a visual stimulus is often reduced by nearby stimuli, an effect known as surround suppression of perceived contrast, which may help in locating the borders of an object. Weaker surround suppression has been observed in schizophrenia but it is unclear whether this abnormality is present in other mental disorders with similar symptomatology, or is evident in people with genetic liability for schizophrenia.

Method.

By examining surround suppression among subjects with schizophrenia or bipolar affective disorder, their unaffected biological relatives and healthy controls we sought to determine whether diminished surround suppression was specific to schizophrenia, and if subjects with a genetic risk for either disorder would show similar deficits. Measuring perceived contrast in different surround conditions also allowed us to investigate how this suppression depends on the similarity of target and surrounding stimuli.

Results.

Surround suppression was weaker among schizophrenia patients regardless of surround configuration. Subjects with bipolar affective disorder showed an intermediate deficit, with stronger suppression than in schizophrenia but weaker than control subjects. Surround suppression was normal in relatives of both patient groups. Findings support a deficit in broadly tuned (rather than sharply orientation- or direction-selective) suppression mechanisms.

Conclusions.

Weak broadly tuned suppression during visual perception is evident in schizophrenia and bipolar affective disorder, consistent with impaired gain control related to the clinical expression of these conditions.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2015 

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

Adesnik, H, Bruns, W, Taniguchi, H, Huang, ZJ, Scanziani, M (2012). A neural circuit for spatial summation in visual cortex. Nature 490, 226231.Google Scholar
Andreasen, NC (1982). Negative symptoms in schizophrenia: definition and reliability. Archives of General Psychiatry 39, 784788.Google Scholar
Andreasen, NC (1984). Scale for the Assessment of Positive Symptoms. University of Iowa: Iowa City, IA.Google Scholar
Andreasen, NC, Pressler, M, Nopoulos, P, Miller, D, Ho, B-C (2010). Antipsychotic dose equivalents and dose-years: a standardized method for comparing exposure to different drugs. Biological Psychiatry 65, 255262.Google Scholar
Angelucci, A, Bressloff, PC (2006). Contribution of feedforward, lateral, and feedback connections to the classical receptive field center and extra-classical receptive field surround of primate V1 neurons. Progress in Brain Research 154, 93120.Google Scholar
APA (2000). Diagnostic and Statistical Manual of Mental Disorders: DSM-IV-TR. American Psychiatric Publishing, Inc.: Washington, DC.Google Scholar
Barch, DM, Carter, CS, Dakin, SC, Gold, J, Luck, SJ, MacDonald, AW, Ragland, JD, Silverstein, S, Strauss, ME (2012). The clinical translation of a measure of gain control: the contrast–contrast effect task. Schizophrenia Bulletin 38, 135143.Google Scholar
Brainard, D (1997). The Psychophysics Toolbox. Spatial Vision 10, 433436.Google Scholar
Butler, PD, Silverstein, S, Dakin, SC (2008). Visual perception and its impairment in schizophrenia. Biological Psychiatry 64, 4047.Google Scholar
Butler, PD, Zemon, V, Schecter, I, Saperstein, AM, Hoptman, MJ, Lim, KO, Revheim, N, Silipo, G, Javitt, DC (2005). Early-stage visual processing and cortical amplification deficits in schizophrenia. Archives of General Psychiatry 62, 495504.Google Scholar
Cavanaugh, JR, Bair, W, Movshon, JA (2002). Selectivity and spatial distribution of signals from the receptive field surround in macaque V1 neurons. Journal of Neurophysiology 88, 25472556.Google Scholar
Chen, Y, Bidwell, LC, Holzman, PS (2005). Visual motion integration in schizophrenia patients, their first-degree relatives, and patients with bipolar disorder. Schizophrenia Research 74, 271281.Google Scholar
Chen, Y, Norton, D, Ongur, D (2008). Altered center-surround motion inhibition in schizophrenia. Biological Psychiatry 64, 7477.Google Scholar
Chen, Y, Norton, D, Stromeyer, C (2014). Prolonged temporal interaction for peripheral visual processing in schizophrenia: evidence from a three-flash illusion. Schizophrenia Research 156, 190196.Google Scholar
Chkonia, E, Roinishvili, M, Makhatadze, N, Tsverava, L, Stroux, A, Neumann, K, Herzog, MH, Brand, A (2010). The shine-through masking paradigm is a potential endophenotype of schizophrenia. PLoS ONE 5, e14268.Google Scholar
Chkonia, E, Roinishvili, M, Reichard, L, Wurch, W, Puhlmann, H, Grimsen, C, Herzog, MH, Brand, A (2012). Patients with functional psychoses show similar visual backward masking deficits. Psychiatry Research 198, 235240.Google Scholar
Dakin, SC, Carlin, P, Hemsley, D (2005). Weak suppression of visual context in chronic schizophrenia. Current Biology 16, R822R824.Google Scholar
First, MB (1997). User's Guide for the Structured Clinical Interview for DSM-IV Axis I Disorders SCID-I: Clinician Version. American Psychiatric Publishing, Inc.: Washington, DC.Google Scholar
Garcia-Perez, MA (1998). Forced-choice staircases with fixed step sizes: asymptotic and small-sample properties. Vision Research 38, 18611881.Google Scholar
Goghari, VM, Sponheim, SR (2008). Divergent backward masking performance in schizophrenia and bipolar disorder: association with COMT. American Journal of Medical Genetics Part B 147B, 223227.Google Scholar
Hashimoto, T, Bazmi, HH, Mirnics, K, Wu, Q, Sampson, AR, Lewis, DA (2008). Conserved regional patterns of GABA-related transcript expression in the neocortex of subjects with schizophrenia. American Journal of Psychiatry 165, 479489.Google Scholar
Hetrick, WP, Erickson, MA, Smith, DA (2012). Phenomenological dimensions of sensory gating. Schizophrenia Bulletin 38, 178191.Google Scholar
Jahshan, C, Wynn, JK, McCleery, A, Glahn, DC, Altshuler, LL, Green, MF (2014). Cross-diagnostic comparison of visual processing in bipolar disorder and schizophrenia. Journal of Psychiatric Research 51, 4248.Google Scholar
Jeyakumar, SLE, Warriner, EM, Raval, VV, Ahmad, SA (2004). Balancing the need for reliability and time efficiency: short forms of the Wechsler Adult Intelligence Scale-III. Educational and Psychological Measurement 64, 7187.Google Scholar
Kelemen, O, Kiss, I, Benedek, G, Kéri, S (2013). Perceptual and cognitive effects of antipsychotics in first-episode schizophrenia: the potential impact of GABA concentration in the visual cortex. Progress in Neuro-Psychopharmacology and Biological Psychiatry 47, 1319.CrossRefGoogle ScholarPubMed
Kéri, DS, Kelemen, O, Benedek, G, Janka, Z (2005). Lateral interactions in the visual cortex of patients with schizophrenia and bipolar disorder. Psychological Medicine 35, 10431051.Google Scholar
Kéri, S, Kelemen, O, Benedek, G, Janka, Z (2001). Different trait markers for schizophrenia and bipolar disorder: a neurocognitive approach. Psychological Medicine 31, 915922.Google Scholar
Kingdom, FAA, Prins, N (2010). Psychophysics: A Practical Introduction. Academic Press: London.Google Scholar
Kraehenmann, R, Vollenweider, FX, Seifritz, E, Kometer, M (2012). Crowding deficits in the visual periphery of schizophrenia patients. PLOS ONE 7, e45884.Google Scholar
Lewis, DA, Hashimoto, T, Volk, DW (2005). Cortical inhibitory neurons and schizophrenia. Nature Reviews Neuroscience 6, 312324.Google Scholar
Ma, W-P, Liu, B-H, Li, Y-T, Huang, ZJ, Zhang, LI, Tao, HW (2010). Visual representations by cortical somatostatin inibitory neurons – selective but with weak and delayed responses. Journal of Neuroscience 30, 1437114379.Google Scholar
Martinez, A, Hillyard, SA, Bickel, S, Dias, EC, Butler, PD, Javitt, DC (2012). Consequences of magnocellular dysfunction on processing attended information in schizophrenia. Cerebral Cortex 22, 12821293.Google Scholar
Martinez, A, Hillyard, SA, Dias, EC, Hagler, DJ, Butler, PD, Guilfoyle, DN, Jalbrzikowski, M, Silipo, G, Javitt, DC (2008). Magnocellular pathway impairment in schizophrenia: evidence from functional magnetic resonance imaging. Journal of Neuroscience 28, 74927500.Google Scholar
Melnick, MD, Harrison, BR, Park, S, Bennetto, L, Tadin, D (2013). A strong interactive link between sensory discriminations and intelligence. Current Biology 23, 10131017.Google Scholar
Must, A, Janka, Z, Benedek, G, Kéri, DS (2004). Reduced facilitation effect of collinear flankers on contrast detection reveals impaired lateral connectivity in the visual cortex of schizophrenia patients. Neuroscience Letters 357, 131134.Google Scholar
Notredame, C-E, Pins, D, Deneve, S, Jardri, R (2014). What visual illusions teach us about schizophrenia. Frontiers in Integrative Neuroscience 8, 63.Google Scholar
Nurminen, L, Angelucci, A (2014). Multiple components of surround modulation in primary visual cortex: multiple neural circuits with multiple functions? Vision Research 104, 4756.Google Scholar
Nurnberger, JI, Blehar, MC, Kaufmann, CA, York-Cooler, C, Simpson, SG, Harkavy-Friedman, J, Severe, JB, Malaspina, D, Reich, T (1994). Diagnostic Interview for Genetic Studies: rationale, unique features, and training. Archives of General Psychiatry 51, 849859.Google Scholar
Overall, JE, Donald, RG (1962). The Brief Psychiatric Rating Scale. Psychological Reports 10, 799812.CrossRefGoogle Scholar
Ozeki, H, Finn, IM, Schaffer, ES, Miller, KD, Ferster, D (2009). Inhibitory stabilization of the cortical network underlies visual surround suppression. Neuron 62, 578592.Google Scholar
Pelli, D (1997). The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spatial Vision 10, 437442.Google Scholar
Phillips, WA, Silverstein, SM (2013). The coherent organization of mental life depends on mechanisms for context-sensitive gain-control that are impaired in schizophrenia. Frontiers in Psychology 4, 307.Google Scholar
Prins, N, Kingdom, FAA (2009). Palamedes: Matlab routines for analyzing psychophysical data. http://www.palamedestoolbox.org Google Scholar
Raine, A (1991). The SPQ: a scale for the assessment of schizotypal personality based on DSM-III-R criteria. Schizophrenia Bulletin 17, 555564.Google Scholar
Robol, V, Tibber, MS, Anderson, EJ, Bobin, T, Carlin, P, Shergill, SS, Dakin, SC (2013). Reduced crowding and poor contour detection in schizophrenia are consistent with weak surround inhibition. PLOS ONE 8, e60951.Google Scholar
Rokem, A, Yoon, JH, Ooms, RE, Maddock, RJ, Minzenberg, MJ, Silver, MA (2011). Broader visual orientation tuning in patients with schizophrenia. Frontiers in Human Neuroscience 5, 127.Google Scholar
Schallmo, M-P, Sponheim, SR, Olman, CA (2013). Abnormal contextual modulation of visual contour detection in patients with schizophrenia. PLOS ONE 8, e68090.Google Scholar
Seymour, K, Stein, T, Sanders, LLO, Guggenmos, M, Theophil, I, Sterzer, P (2013). Altered contextual modulation of primary visual cortex responses in schizophrenia. Neuropsychopharmacology 38, 26072612.CrossRefGoogle ScholarPubMed
Skottun, BC, Skoyles, JR (2007). Contrast sensitivity and magnocellular functioning in schizophrenia. Vision Research 47, 29232933.Google Scholar
Sponheim, SR, Sass, SM, Noukki, AL, Hegeman, BM (2013). Fragile early visual percepts mark genetic liability specific to schizophrenia. Schizophrenia Bulletin 39, 839847.Google Scholar
Tadin, D, Kim, J, Doop, ML, Gibson, C, Lappin, JS, Blake, R, Park, S (2006). Weakened center-surround interactions in visual motion processing in schizophrenia. Journal of Neuroscience 24, 1140311412.Google Scholar
Tibber, MS, Anderson, EJ, Bobin, T, Antonova, E, Seabright, A, Wright, B, Carlin, P, Shergill, S, Dakin, SC (2013). Visual surround suppression in schizophrenia. Frontiers in Psychology 4, 113.Google Scholar
Uhlhaas, PJ, Silverstein, SM, Phillips, WA, Lovell, PG (2004). Evidence for impaired visual context processing in schizotypy with thought disorder. Schizophrenia Research 68, 249260.Google Scholar
Webb, BS, Dhruv, NT, Solomon, SG, Tailby, C, Lennie, P (2005). Early and late mechanisms of surround suppression in striate cortex of macaque. Journal of Neuroscience 25, 1166611675.Google Scholar
Williams, AL, Singh, KD, Smith, AT (2003). Surround modulation measured with functional MRI in the human visual cortex. Journal of Neurophysiology 89, 525533.Google Scholar
Wilson, S, Sponheim, SR (2014). Dimensions underlying psychotic and manic symptomatology: extending normal-range personality traits to schizophrenia and bipolar spectra. Comprehensive Psychiatry 55, 18091819.Google Scholar
Xing, J, Heeger, DJ (2000). Center-surround interactions in foveal and peripheral vision. Vision Research 40, 30653072.Google Scholar
Yang, E, Tadin, D, Glasser, DM, Hong, SW, Blake, R, Park, S (2013 a). Visual context processing in bipolar disorder: a comparison with schizophrenia. Frontiers in Psychology 4, 112.Google Scholar
Yang, E, Tadin, D, Glasser, DM, Hong, SW, Blake, R, Park, S (2013 b). Visual context processing in schizophrenia. Clinical Psychological Science 1, 515.Google Scholar
Yoon, JH, Maddock, RJ, Rokem, A, Silver, MA, Minzenberg, MJ, Ragland, JD, Carter, CS (2010). GABA concentration is reduced in visual cortex in schizophrenia and correlates with orientation-specific surround suppression. Journal of Neuroscience 30, 37773781.Google Scholar
Yoon, JH, Rokem, AS, Silver, MA, Minzenberg, MJ, Ursu, S, Ragland, JD, Carter, CS (2009). Diminished orientation-specific surround suppression of visual processing in schizophrenia. Schizophrenia Bulletin 35, 10781084.Google Scholar
Yoon, JH, Sheremata, SL, Rokem, A, 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, 681.Google Scholar
Yu, C, Klein, SA, Levi, DM (2001). Surround modulation of perceived contrast and the role of brightness induction. Journal of Vision 1, 1831.Google Scholar