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Subcortical visual dysfunction in schizophrenia drives secondary cortical impairments
Open accessAbstract
Visual processing deficits are an integral component of schizophrenia and are sensitive predictors of schizophrenic decompensation in healthy adults. The primate visual system consists of discrete subcortical magnocellular and parvocellular pathways, which project preferentially to dorsal and ventral cortical streams. Subcortical systems show differential stimulus sensitivity, while cortical systems, in turn, can be differentiated using surface potential analysis. The present study examined contributions of subcortical dysfunction to cortical processing deficits using high-density event-related potentials. Event-related potentials were recorded to stimuli biased towards the magnocellular system using low-contrast isolated checks in Experiment 1 and towards the magnocellular or parvocellular system using low versus high spatial frequency (HSF) sinusoidal gratings, respectively, in Experiment 2. The sample consisted of 23 patients with schizophrenia or schizoaffective disorder and 19 non-psychiatric volunteers of similar age. In Experiment 1, a large decrease in the P1 component of the visual event-related potential in response to magnocellular-biased isolated check stimuli was seen in patients compared with controls (F = 13.2, P = 0.001). Patients also showed decreased slope of the contrast response function over the magnocellular-selective contrast range compared with controls (t = 9.2, P = 0.04) indicating decreased signal amplification. In Experiment 2, C1 (F = 8.5, P = 0.007), P1 (F = 33.1, P < 0.001) and N1 (F = 60.8, P < 0.001) were reduced in amplitude to magnocellular-biased low spatial frequency (LSF) stimuli in patients with schizophrenia, but were intact to parvocellular-biased HSF stimuli, regardless of generator location. Source waveforms derived from inverse dipole modelling showed reduced P1 in Experiment 1 and reduced C1, P1 and N1 to LSF stimuli in Experiment 2, consistent with surface waveforms. These results indicate pervasive magnocellular dysfunction at the subcortical level that leads to secondary impairment in activation of cortical visual structures within dorsal and ventral stream visual pathways. Our finding of early visual dysfunction is consistent with and explanatory of classic literature showing subjective complaints of visual distortions and is consistent with early visual processing deficits reported in schizophrenia. Although deficits in visual processing have frequently been construed as resulting from failures of top-down processing, the present findings argue strongly for bottom-up rather than top-down dysfunction at least within the early visual pathway. Deficits in magnocellular processing in this task may reflect more general impairments in neuronal systems functioning, such as deficits in non-linear amplification and may thus represent an organizing principle for predicting neurocognitive dysfunction in schizophrenia.
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“Second, patients show reduced amplitude responses to simple visual stimuli with steady-state or transient electrophysiological techniques (21,22), indicating deficits in contrast gain control within the early visual system.”
From Visual perception and its impairment in schizophrenia (2008) · cites this paper as [21]
In the citing paper
“Patients with schizophrenia show preferential M-pathway dysfunction (21,22,28,35–38), although deficits have also been observed in parvocellular processing (19,20).”
From Visual perception and its impairment in schizophrenia (2008) · cites this paper as [21]
In the citing paper
“Second, patients show reduced amplitude responses to simple visual stimuli with steady-state or transient electrophysiological techniques (21,22), indicating deficits in contrast gain control within the early visual system.”
From Visual perception and its impairment in schizophrenia (2008) · cites this paper as [21]
In the citing paper
“Neurophysiological studies have demonstrated impaired generation of the visual P1 potential to stimuli biased toward the magnocellular visual system (65, 89–91)”
From Sensory Processing Dysfunction in the Personal Experience and Neuronal Machinery of Schizophrenia (2015) · cites this paper as [90]
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“Disruptions within this network have been associated with SZ-related symptoms such as sensory gating deficits, psychomotor disturbances, and perceptual abnormalities (Butler et al 2007, Liddle and Sami 2024).”
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ERP Components: *and Downs of Brainwave Recordings
Kappenman, E. S., & Luck, S. J. (2011)
The role of cognitive control in memory retrievalapplications to schizotypy and schizophrenia
Doidge, A. N. (2015) · ORCA Online Research @Cardiff (Cardiff University)
Early Visual Processing Abnormalities Related to Schizophrenia and Autism Spectrum Disorder
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Shah, D. K. (2018) · uO Research (University of Ottawa) · doi:10.20381/ruor-22753
“5 ERP Correlates of Emotional Facial Processing in Schizophrenia Deficits in P100 component in patients with schizophrenia have been observed with nonface stimuli (Butler et al., 2007; Doniger, Foxe, Murray, Higgins & Javitt, 2002; Haenschel et al., 2007; Schechter et al., 2005; Yeap et al., 2006), but results are mix…”
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“Unlike prior reports of broad subcortical-visual abnormalities (Butler et al., 2007), our findings specifically demonstrate disrupted inhibitory interactions between these domains, offering more precise mechanistic insights.”
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Self-citationОсобенности нейрокогнитивного функционирования при шизотипическом расстройстве и шизофрении
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“The visual processing deficits in schizophrenia are explained most parsimoniously by impaired N -methyl-D-aspartate receptor (NMDAR)-function within subcortical and early visual regions (Butler et al., 2005; Butler et al., 2007; Javitt, 2015).”
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Metadata
- Authors
- Butler, P. D., Martinez, A., Foxe, J. J., Kim, D., Zemon, V., Silipo, G., Mahoney, J., Shpaner, M., Jalbrzikowski, M., & Javitt, D. C.
- Affiliations
- Nathan Kline Institute for Psychiatric Research (US)
- Yeshiva University (US)
- Corresponding author
- Butler, P. D.
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 2007-02-01
- Volume
- 130
- Issue
- 2
- Pages
- 417-430
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- PMC
- PMC2072909
- OpenAlex
- W2135837826
- Cited by
- 292
- References
- 117
- Citations by year
- 2026: 5 · 2025: 9 · 2024: 9 · 2023: 14 · 2022: 8 · 2021: 14 · 2020: 15 · 2019: 11 · 2018: 13 · 2017: 14 · 2016: 13 · 2015: 16 · 2014: 16 · 2013: 22 · 2012: 19
- FWCI
- 11.29
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Brain (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Alliance for Research on Schizophrenia and Depression
- Wellcome Trust
- U.S. Public Health Service (MH49334)
- National Institute of Mental Health (R37MH049334, R37MH49334, R01MH066374, K02-MH-01439, R01-MH65350, R01MH065350, R03MH067579, MH66374, K02MH001439)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Hallucinations in medical conditions
- Keywords
- schizophrenia, visual processing deficits, magnocellular pathway, parvocellular pathway, dorsal and ventral visual streams, P1 component, contrast response function, spatial frequency, bottom-up processing, schizoaffective disorder, visual distortion, event-related potentials, top-down processing, decompensation prediction
- MeSH terms
- Adult, Brain Mapping, Electroencephalography, Evoked Potentials, Visual, Female, Humans, Male, Pattern Recognition, Visual, Photic Stimulation, Psychiatric Status Rating Scales, Reaction Time, Schizophrenia, Schizophrenic Psychology, Visual Pathways, Contrast Sensitivity, Basal Nucleus of Meynert
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