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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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Lisman, J. E., Coyle, J. T., Green, R. W., Javitt, D. C., Benes, F. M., Heckers, S., & Grace, A. A. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.02.005 · Cited by 1,010
Self-citationPsychosis and autism as diametrical disorders of the social brain
Crespi, B. J., & Badcock, C. R. (2008) · Behavioral and Brain Sciences · doi:10.1017/s0140525x08004214 · Cited by 635
“…cascades of perturbed development comes from studies of schizophrenia demonstrating deficits in early sensory processing (Butler & Javitt 2005; Butler et al. 2007; Uhlhaas & Silverstein 2005) and relating auditory frequency discrimination to deficits in affect recognition (Leitman et al.…”
BackgroundWhen Doors of Perception Close: Bottom-up Models of Disrupted Cognition in Schizophrenia
Javitt, D. C. (2009) · Annual Review of Clinical Psychology · doi:10.1146/annurev.clinpsy.032408.153502 · Cited by 503
“Thus, whereas deficits are expressed over dorsal versus ventral stream, as with ssVEP, the deficits appear to be driven by impairments arising subcortically within the magno-versus parvocellular pathways (Butler et al. 2007).”
BackgroundSelf-citationVisual perception and its impairment in schizophrenia
Butler, P. D., Silverstein, S. M., & Dakin, S. C. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.03.023 · Cited by 472
Self-citationSensory Processing Dysfunction in the Personal Experience and Neuronal Machinery of Schizophrenia
Javitt, D. C., & Freedman, R. (2015) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2014.13121691 · Cited by 403
Self-citationMagnocellular Projections as the Trigger of Top-Down Facilitation in Recognition
Kveraga, K., Boshyan, J., & Bar, M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3481-07.2007 · Cited by 429
“…have been shown in the past to be effective in studying visual search and attention (Steinman et al., 1997; Cheng et al., 2004) and M- and P-biased letter and mask stimuli have also been used in studying visual perception abnormalities in schizophrenia (Schechter et al., 2003; Butler et al., 2006).”
MethodKantrowitz, J. T., & Javitt, D. C. (2010) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2010.04.006 · Cited by 414
Self-citationTop-down predictions in the cognitive brain
Kveraga, K., Ghuman, A. S., & Bar, M. (2007) · Brain and Cognition · doi:10.1016/j.bandc.2007.06.007 · Cited by 423
“…the role of the M pathway in directing spatial attention (Steinman, Steinman, & Garzia, 1998; Steinman, Steinman, & Lehmkuhle, 1997) and visual search (Cheng, Eysel, & Vidyasagar, 2004), as well as to detect the M-pathway impairments in schizophrenia (Butler et al., 2007; Schechter et al., 2005).”
BackgroundMethodInfluentialSensory Processing in Schizophrenia: Neither Simple nor Intact
Javitt, D. C. (2009) · Schizophrenia Bulletin · doi:10.1093/schbul/sbp110 · Cited by 328
Self-citationCognitive Training for Impaired Neural Systems in Neuropsychiatric Illness
Vinogradov, S., Fisher, M., & de Villers‐Sidani, E. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.251 · Cited by 345
“Though these have been particularly well studied in schizophrenia (Butler et al, 2007; Javitt, 2009; Dias et al, 2011), they are also present in bipolar disorder, in depression, in PTSD, in alcoholism, in cocaine addiction, in ADD, in autism, and in the aging brain (Table 4).”
BackgroundEarly-stage visual processing deficits in schizophrenia
Butler, P. D., & Javitt, D. C. (2005) · Current Opinion in Psychiatry · doi:10.1097/00001504-200503000-00008 · Cited by 294
Self-citationGlutamatergic theories of schizophrenia.
Javitt, D. C. (2010) · PubMed · Cited by 248
Self-citationVisual symptoms in Parkinson's disease and Parkinson's disease dementia
Archibald, N. K., Clarke, M. P., Mosimann, U. P., & Burn, D. J. (2011) · Movement Disorders · doi:10.1002/mds.23891 · Cited by 220
Martı́nez, A., Hillyard, S. A., Dias, E. C., Hagler, D. J., Butler, P. D., Guilfoyle, D. N., Jalbrzikowski, M., Silipo, G. S., & Javitt, D. C. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1852-08.2008 · Cited by 205
“Additionally, the amplitudes of sensory-evoked ERPs elicited by low, but not high, SFs are reduced in patients compared with control subjects (Butler et al., 2007).”
BackgroundResultSelf-citationMultimodal Neuroimaging in Schizophrenia: Description and Dissemination
Aine, C. J., Bockholt, H. J., Bustillo, J., Cañive, J. M., Caprihan, A., Gasparovic, C., Hanlon, F. M., Houck, J. M., Jung, R. E., Lauriello, J., et al. (2017) · Neuroinformatics · doi:10.1007/s12021-017-9338-9 · Cited by 196
“In addition, due to a reported deficit in the visual dorsal stream in SP (Butler et al. 2007, Butler et al. 2005, Doniger et al. 2002, Foxe et al. 2001, 2005, Kim et al. 2006, 2005, O'Donnell et al. 1996, Schechter et al. 2006, 2005), a neural circuit sensitive to the spatial location of objects,…”
BackgroundRoss, L. A., Saint‐Amour, D., Leavitt, V. M., Molholm, S., Javitt, D. C., & Foxe, J. J. (2007) · Schizophrenia Research · doi:10.1016/j.schres.2007.08.008 · Cited by 188
“, 2001) and electrophysiological studies have shown early dorsal visual stream processing deficits in schizophrenia (Doniger et al., 2002; Foxe et al., 2001, 2005; Yeap et al., 2006; Butler et al., 2007) that may well be the origin for impairment of “upstream” function involving motion perception (Chen et al.”
BackgroundSelf-citationSensory Contributions to Impaired Emotion Processing in Schizophrenia
Butler, P. D., Abeles, I. Y., Weiskopf, N. G., Tambini, A., Jalbrzikowski, M., Legatt, M. E., Zemon, V. M., Loughead, J., Gur, R. C., & Javitt, D. C. (2009) · Schizophrenia Bulletin · doi:10.1093/schbul/sbp109 · Cited by 149
Self-citationDifferences in early sensory-perceptual processing in synesthesia: A visual evoked potential study
Barnett, K. J., Foxe, J. J., Molholm, S., Kelly, S. P., Shalgi, S., Mitchell, K. J., & Newell, F. N. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.07.028 · Cited by 148
“Butler et al. (2007) argue that bottom-up processing deficits in the magnocellular system might be responsible for visuo-perceptual differences in schizophrenia .”
Self-citationVisual Perception Disturbances in Schizophrenia: A Unified Model
Silverstein, S. M. (2016) · Nebraska Symposium on Motivation/The Nebraska symposium on motivation · doi:10.1007/978-3-319-30596-7_4 · Cited by 147
“6 Responses to these criticisms were published by Butler et al. ( 2007 ) and Keri and Benedek ( 2012 ).”
BackgroundEarly Sensory Contributions to Contextual Encoding Deficits in Schizophrenia
Dias, E. C., Butler, P. D., Hoptman, M. J., & Javitt, D. C. (2011) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2011.17 · Cited by 139
Self-citationRETRACTED: Impaired Visual Cortical Plasticity in Schizophrenia
Çavuş, I., Reinhart, R. M. G., Roach, B. J., Gueorguieva, R., Teyler, T. J., Clapp, W. C., Ford, J. M., Krystal, J. H., & Mathalon, D. H. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.01.013 · Cited by 130
“Moreover, while a P1 component is often prominent following the C1 (54, 66), we observed a small bilateral P1 peaking 15 ms earlier than the midline C1 (Figure 2), replicating Butler’s data (65).”
BackgroundResultRetractedDickinson, D., & Harvey, P. D. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn097 · Cited by 138
Compressed sensorimotor-to-transmodal hierarchical organization in schizophrenia
Dong, D., Yao, D., Wang, Y., Hong, S., Genon, S., Xin, F., Jung, K., He, H., Chang, X., Duan, M., et al. (2021) · Psychological Medicine · doi:10.1017/s0033291721002129 · Cited by 138
“However, a growing number of studies demonstrate basic auditory and visual deficits significantly contribute to higher-order cognitive dysfunctions (Butler et al., 2007, 2009; Calderone et al., 2013; Dias, Butler, Hoptman, & Javitt, 2011; Dondé et al., 2019; Hoptman et al., 2018; Leitman et al.,…”
Sehatpour, P., Dias, E. C., Butler, P. D., Revheim, N., Guilfoyle, D. N., Foxe, J. J., & Javitt, D. C. (2010) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2010.85 · Cited by 134
“Here,asinpreviousstudies,theearliestdeficitswerefound in generation of the dorsal stream P1 potential, suggesting failureofmagnocellularand/orearly-stagecorticalprocessing, followedby impairedgenerationofNCL.(17,37,38) Although corticalvisualareaV1activationwasnotassessedinthisstudy relative to fragmented images, pati…”
BackgroundSelf-citationNeural mechanisms of mismatch negativity dysfunction in schizophrenia
Lee, M., Sehatpour, P., Hoptman, M. J., Lakatos, P., Dias, E. C., Kantrowitz, J. T., Martı́nez, A., & Javitt, D. C. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.3 · Cited by 126
Self-citationContrast sensitivity and magnocellular functioning in schizophrenia
SKOTTUN, B. C., & Skoyles, J. R. (2007) · Vision Research · doi:10.1016/j.visres.2007.07.016 · Cited by 112
Mismatch negativity as a biomarker of theta band oscillatory dysfunction in schizophrenia
Javitt, D. C., Lee, M., Kantrowitz, J. T., & Martı́nez, A. (2017) · Schizophrenia Research · doi:10.1016/j.schres.2017.06.023 · Cited by 115
Self-citationThalamocortical connectivity during resting state in schizophrenia
Klingner, C. M., Langbein, K., Dietzek, M., Smesny, S., Witte, O. W., Sauer, H., & Nenadić, I. (2013) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-013-0417-0 · Cited by 111
Foxe, J. J., Strugstad, E. C., Sehatpour, P., Molholm, S., Pasieka, W., Schroeder, C. E., & McCourt, M. E. (2008) · Brain Topography · doi:10.1007/s10548-008-0063-4 · Cited by 106
“Schwartz et al. 2001; Butler et al. 2001, 2007; Foxe et al. 2001, 2005a, b; Yeap et al. 2006; Lalor et al. 2008).”
Self-citationFriedman, T., Sehatpour, P., Dias, E., Perrin, M., & Javitt, D. C. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.10.037 · Cited by 102
“The electrodes for each component were chosen based upon visual inspection of the data and published distributions of auditory and visual ERPs (44, 52).”
MethodInfluentialSelf-citationWynn, J. K., Lee, J., Horan, W. P., & Green, M. F. (2007) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn047 · Cited by 102
Consequences of Magnocellular Dysfunction on Processing Attended Information in Schizophrenia
Martinez, A., Hillyard, S. A., Bickel, S., Dias, E. C., Butler, P. D., & Javitt, D. C. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhr195 · Cited by 94
“In recent years, deficits in early visual processing have been increasingly documented in schizophrenia (Butler et al. 2005, 2007; Martinez et al. 2008), and it has been suggested that these sensory processing deficits may play a role in impaired functioning of higher order cognitive mechanisms.”
BackgroundMethodResultInfluentialSelf-citationSeeing the World Dimly: The Impact of Early Visual Deficits on Visual Experience in Schizophrenia
Kantrowitz, J. T., Butler, P. D., Schecter, I., Silipo, G. S., & Javitt, D. C. (2009) · Schizophrenia Bulletin · doi:10.1093/schbul/sbp100 · Cited by 97
Self-citationVisual sensory processing deficits in Schizophrenia and their relationship to disease state
Yeap, S., Kelly, S. P., Sehatpour, P., Magno, E., Garavan, H., Thakore, J. H., & Foxe, J. J. (2008) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-008-0802-2 · Cited by 89
“Clearly this is speculative and it should be pointed out that the P1 deficit has also been linked to excitatory (n-methyld-aspartate (NMDA)) functioning (see [ 9 ]).”
Self-citationNeurophysiological models for new treatment development in schizophrenia: early sensory approaches
Javitt, D. C. (2015) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12689 · Cited by 84
Self-citationCalderone, D., Hoptman, M. J., Martı́nez, A., Nair-Collins, S., Mauro, C. J., Bar, M., Javitt, D. C., & Butler, P. D. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs169 · Cited by 83
Self-citationVolume and neuron number of the lateral geniculate nucleus in schizophrenia and mood disorders
Dorph‐Petersen, K., Carić, D., Saghafi, R., Zhang, W., Sampson, A. R., & Lewis, D. A. (2008) · Acta Neuropathologica · doi:10.1007/s00401-008-0410-2 · Cited by 79
“ment of the visual system in subjects with schizophrenia described in the literature [15, 16, 23, 48, 53].”
Review of neurophysiological findings in patients with schizophrenia
Onitsuka, T., Oribe, N., Nakamura, I., & Kanba, S. (2013) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.12090 · Cited by 85
“For example, it was reported that patients showed reduced P100 amplitude in response to nonface stimuli,(61) and face stimuli, compared with healthy subjects.(62) A reduction in P100 amplitude was also reported in studies using M-pathway-biased stimuli, while studies using P-pathway-biased stimuli did not observe such…”
ResultRetinal Layer Abnormalities as Biomarkers of Schizophrenia
Samani, N. N., Proudlock, F. A., Siram, V., Suraweera, C. U., Hutchinson, C. V., Nelson, C. P., Al-Uzri, M. M., & Gottlob, I. (2017) · Schizophrenia Bulletin · doi:10.1093/schbul/sbx130 · Cited by 80
Lencer, R., Sprenger, A., Reilly, J. L., McDowell, J. E., Rubin, L. H., Badner, J. A., Keshavan, M. S., Pearlson, G. D., Tamminga, C. A., Gershon, E. S., et al. (2015) · Schizophrenia Research · doi:10.1016/j.schres.2015.09.032 · Cited by 73
“These findings are broadly consistent with models proposing that visual information processing deficits represent a core feature of psychotic disorders (Butler et al., 2007; Yoon et al., 2013).”
ResultEarly-stage visual perception impairment in schizophrenia, bottom-up and back again
Adámek, P., Langová, V., & Horáček, J. (2022) · Schizophrenia · doi:10.1038/s41537-022-00237-9 · Cited by 88
Wölwer, W., Brinkmeyer, J., Stroth, S., Streit, M., Bechdolf, A., Ruhrmann, S., Wagner, M., & Gäebel, W. (2011) · Schizophrenia Bulletin · doi:10.1093/schbul/sbr013 · Cited by 68
Lee, S., Kim, E. Y., Kim, S., & Bae, S. (2010) · Neuroscience Research · doi:10.1016/j.neures.2010.03.001 · Cited by 66
Neurophysiological and neurochemical animal models of schizophrenia: Focus on glutamate☆
Bickel, S., & Javitt, D. C. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.05.005 · Cited by 68
“An increasing body of evidence indicates that neural deficits in patients affect not only higher cognitive functions, such as memory, executive functions, and attention, but also early sensory processes within the auditory and visual (among other sensory) modalities [17,49].”
BackgroundSelf-citationAn event-related potential examination of contour integration deficits in schizophrenia
Butler, P. D., Abeles, I. Y., Silverstein, S. M., Dias, E. C., Weiskopf, N. G., Calderone, D., & Sehatpour, P. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00132 · Cited by 69
“Decreased P1 has also been seen in a number of studies of schizophrenia (Yeap et al., 2006; Butler et al., 2007; Haenschel et al., 2007; Dias et al., 2011; Martinez et al., 2011), and is thought to reflect impaired magnocellular and/or early-stage cortical processing (Butler et al.”
BackgroundInfluentialSelf-citationSKOTTUN, B. C. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.07.002 · Cited by 69
Koychev, I. G., El‐Deredy, W., Haenschel, C., & Deakin, J. F. W. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2010.04.014 · Cited by 62
“The P1 reduction has been linked to impairment in the magnocellular visual pathway (Butler et al., 2007; Foxe et al., 2001) and data from psychophysical studies support this association (Keri et al., 2002; Keri et al., 1998; Keri, Kelemen, Janka, & Benedek, 2005; Schwartz, Tomlin, Evans, & Ross,…”
MethodFrey, H., Molholm, S., Lalor, E. C., Russo, N. N., & Foxe, J. J. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12243 · Cited by 63
“Essen, 1984) we also employed stimuli specifically biased towards activation of magnocellular neurons (Butler et al., 2007; Foxe et al., 2008; Lalor & Foxe, 2009).”
MethodSelf-citationJemel, B., Mimeault, D., Saint‐Amour, D., Hosein, A., & Mottron, L. (2010) · Journal of Vision · doi:10.1167/10.6.13 · Cited by 61
“It is generally accepted that VEPs provide an objective evaluation of visual resolution and contrast sensitivity in human adults and infants (Fiorentini, Pirchio, & Spinelli, 1980; Norcia & Tyler, 1985; Regan, 1989) and the integrity of cortical visual channels in several clinical conditions (Butler et al., 2007).”
BackgroundDisambiguating the roles of area V1 and the lateral occipital complex (LOC) in contour integration
Shpaner, M., Molholm, S., Forde, E., & Foxe, J. J. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.11.023 · Cited by 61
“Prior studies reported modulations of the C1 component ranging from 20 to 50% in response to different levels of luminance contrast (e.g., Butler et al., 2007) as well as in the context of attentional amplification (Kelly et al., 2008) and multisensory integration (Molholm et al., 2002).”
BackgroundSelf-citationWhat's in a face? Effects of stimulus duration and inversion on face processing in schizophrenia
Butler, P. D., Tambini, A., Yovel, G., Jalbrzikowski, M., Ziwich, R., Silipo, G. S., Kanwisher, N., & Javitt, D. C. (2008) · Schizophrenia Research · doi:10.1016/j.schres.2008.03.007 · Cited by 61
“stream cortical regions, or because of impaired input from subcortical visual systems (Butler et al., 2007).”
BackgroundResultInfluentialSelf-citationStone, D. B., Urrea, L. J., Aine, C. J., Bustillo, J., Clark, V. P., & Stephen, J. M. (2011) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2011.07.017 · Cited by 54
“Processing deficits have also been detected in several early components of the visual evoked potential (VEP), such as the C1 (Butler et al., 2007) and the P1 components (Butler et al., 2007; Foxe, Doniger, & Javitt, 2001).”
BackgroundObayashi, C., Nakashima, T., Onitsuka, T., Maekawa, T., Hirano, Y., Hirano, S., Oribe, N., Kaneko, K., Kanba, S., & Tobimatsu, S. (2009) · Clinical Neurophysiology · doi:10.1016/j.clinph.2009.06.016 · Cited by 58
Efference Copy Failure during Smooth Pursuit Eye Movements in Schizophrenia
Spering, M., Dias, E. C., Sanchez, J. L., Schütz, A. C., & Javitt, D. C. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0578-13.2013 · Cited by 61
Self-citationCalderone, D., Martı́nez, A., Zemon, V. M., Hoptman, M. J., Hu, G., Watkins, J. E., Javitt, D. C., & Butler, P. D. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.11.019 · Cited by 54
“The shape of the curves is consistent with nonlinear gain in the magnocellular-biased condition and supports previous studies (Butler et al., 2001, 2005, 2007, 2008a; Green et al., 2009; Zemon and Gordon, 2006) that show schizophrenia is associated with specific deficits in contrast gain.”
ResultSelf-citationSaito, R., Koebis, M., Nagai, T., Shimizu, K., Liao, J., Wulaer, B., Sugaya, Y., Nagahama, K., Uesaka, N., Kushima, I., et al. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-0723-z · Cited by 63
Landgraf, S., & Osterheider, M. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00352 · Cited by 58
“These mechanisms, in turn, have been described as relevant for the development of schizophrenia (Butler et al., 2005, 2007; Johnson et al., 2005; Kim et al., 2005; Haenschel et al., 2007).”
BackgroundRivolta, D., Castellanos, N. P., Stawowsky, C., Helbling, S., Wibral, M., Grützner, C., Koethe, D., Birkner, K., Kranaster, L., Enning, F., et al. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.3752-13.2014 · Cited by 58
“Although previous work has highlighted impairments in dorsal stream functioning underlying early visual processing deficits (Doniger et al., 2002; Butler et al., 2007), the high-contrast levels of Mooney faces are mainly targeting parvocellular pathways that project predominantly to the ventral…”
BackgroundHigh-frequency neural oscillations and visual processing deficits in schizophrenia
Tan, H. M., Lana, L., & Uhlhaas, P. J. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00621 · Cited by 53
“…cues (Silverstein et al., 1996) as well as dysfunctions in bottom-up driven processing in early visual pathways (Uhlhaas and Silverstein, 2005; Butler et al., 2007), suggesting that effects of attention on neural oscillations could be relevant in order to disentangle the contribution of…”
Backgroundvan de Ven, V. G., Rotarska-Jagiela, A., Oertel‐Knöchel, V., & Linden, D. E. J. (2017) · NeuroImage Clinical · doi:10.1016/j.nicl.2017.04.012 · Cited by 52
“Reports of diminished magnocellular pathway responses (Butler et al., 2007, 2005; Martinez et al., 2008), impaired performance in visual contextual tasks (Dakin et al., 2005; Yoon et al., 2009) and visual illusions (Kantrowitz et al., 2009) indicate deficits in neural pathways at the level of…”
InfluentialNuechterlein, K. H., Ventura, J., Subotnik, K. L., Hayata, J. N., Medalia, A. A., & Bell, M. D. (2014) · American Journal of Psychiatric Rehabilitation · doi:10.1080/15487768.2014.935674 · Cited by 53
“on low-level sensory, perceptual, and other preattentive processing deficits in schizophrenia, it is difficult to believe that training primarily higher-order processes would fundamentally resolve deficits in low-level sensory and perceptual processing (Butler et al., 2007; Javitt, 2009).”
BackgroundAbnormal Superior Temporal Connectivity During Fear Perception in Schizophrenia
Leitman, D. I., Loughead, J., Wolf, D. H., Ruparel, K., Kohler, C. G., Elliott, M. A., Bilker, W. B., Gur, R. E., & Gur, R. C. (2007) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn052 · Cited by 55
Generating Controlled Image Sets in Cognitive Neuroscience Research
Knebel, J.-F., Toepel, U., Hudry, J., le Coutre, J., & Murray, M. M. (2008) · Brain Topography · doi:10.1007/s10548-008-0046-5 · Cited by 49
Cadenhead, K. S., Dobkins, K. R., McGovern, J. E., & Shafer, K. M. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00535 · Cited by 49
“…interaction extends into the dorsal and ventral streams occurring thereafter (Kovacs et al., 1995; Sawatari and Callaway, 1996; Keri et al., 2000; Butler et al., 2007; Skottun and Skoyles, 2007) making it difficult to conclude from the VBM paradigm alone whether there are specific subcortical…”
BackgroundResultGrent-‘t-Jong, T., Rivolta, D., Sauer, A., Grube, M., Singer, W., Wibral, M., & Uhlhaas, P. J. (2016) · Schizophrenia Research · doi:10.1016/j.schres.2016.06.003 · Cited by 52
“, 1995), physiology (Rivolta et al, 2014; Sun et al., 2013; Grützner et al., 2013; Krishnan et al., 2005; Butler et al., 2007) and psychophysics (Butler et al.”
BackgroundLalor, E. C., Yeap, S., Reilly, R. B., Pearlmutter, B. A., & Foxe, J. J. (2007) · Schizophrenia Research · doi:10.1016/j.schres.2007.09.037 · Cited by 47
“…relatively severe deficits in early visual sensory processing, as indexed by a robust decrement in amplitude of the occipital P1 component (e.g., Foxe et al., 2001, 2005; Butler et al., 2001, 2007; Doniger et al., 2002; Spencer et al., 2003; Schechter et al., 2005; Haenschel et al., in press).”
BackgroundResultInfluentialSelf-citationLeavitt, V. M., Molholm, S., Ritter, W., Shpaner, M., & Foxe, J. J. (2007) · Journal of Psychiatry and Neuroscience · doi:10.1139/jpn.0734 · Cited by 44
Self-citationImpaired magnocellular/dorsal stream activation predicts impaired reading ability in schizophrenia
Martínez, A., Revheim, N., Butler, P. D., Guilfoyle, D. N., Dias, E. C., & Javitt, D. C. (2013) · NeuroImage: Clinical · doi:10.1016/j.nicl.2012.09.006 · Cited by 45
“, 2005) and transient (Butler et al., 2007; Schechter et al., 2005) event-related potentials (ERPs), and with functional neuroimaging (fMRI) measures (Martinez et al.”
Self-citationRünker, A. E., O’Tuathaigh, C. M. P., Dunleavy, M., Morris, D. W., Little, G. E., Corvin, A. P., Gill, M., Henshall, D. C., Waddington, J. L., & Mitchell, K. J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0026488 · Cited by 52
“cortex [6,61,75,76] and a reduction in the size of primary visual cortex [77], both of which are observed in adult Sema6A mutants”
Oribe, N., Hirano, Y., Kanba, S., del Re, E. C., Seidman, L. J., Mesholam‐Gately, R. I., Spencer, K., McCarley, R. W., & Niznikiewicz, M. A. (2013) · Schizophrenia Research · doi:10.1016/j.schres.2013.01.015 · Cited by 50
“For example, P1 reduction was reported in studies using magnocellular pathway biased stimuli (low contrast/ spatial frequency) while studies using parvocellular pathway biased stimuli (high contrast/spatial frequency) did not find the reduction (Butler et al., 2007).”
Is Attentional Filtering Impaired in Schizophrenia?
Luck, S. J., Leonard, C. J., Hahn, B., & Gold, J. M. (2019) · Schizophrenia Bulletin · doi:10.1093/schbul/sbz045 · Cited by 42
Impaired early visual response modulations to spatial information in chronic schizophrenia
Knebel, J., Javitt, D. C., & Murray, M. M. (2011) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2011.02.006 · Cited by 45
Self-citationImpaired Working Memory Capacity Is Not Caused by Failures of Selective Attention in Schizophrenia
Erickson, M. A., Hahn, B., Leonard, C. J., Robinson, B. M., Gray, B., Luck, S. J., & Gold, J. M. (2014) · Schizophrenia Bulletin · doi:10.1093/schbul/sbu101 · Cited by 43
Current Trends in the Empirical Study of Cognitive Remediation for Schizophrenia
Saperstein, A. M., & Kurtz, M. M. (2013) · The Canadian Journal of Psychiatry · doi:10.1177/070674371305800602 · Cited by 46
Neural oscillatory deficits in schizophrenia predict behavioral and neurocognitive impairments
Martı́nez, A., Gaspar, P. A., Hillyard, S. A., Bickel, S., Lakatos, P., Dias, E. C., & Javitt, D. C. (2015) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2015.00371 · Cited by 44
“These ERP results were paralleled by reduced functional MRI activation and differential behavioral deficits (e.g., reduced hit rate) for LSF compared to HSF stimuli, consistent with a selective magnocellular pathway dysfunction (see also Butler et al., 2001, 2007; Martínez et al., 2008).”
BackgroundResultSelf-citationOribe, N., Hirano, Y., Kanba, S., del Re, E. C., Seidman, L. J., Mesholam-Gately, R. I., Goldstein, J. M., Shenton, M. E., Spencer, K., McCarley, R. W., et al. (2014) · Schizophrenia Bulletin · doi:10.1093/schbul/sbu083 · Cited by 44
Abnormalities in the effective connectivity of visuothalamic circuitry in schizophrenia
Iwabuchi, S. J., & Palaniyappan, L. K. (2017) · Psychological Medicine · doi:10.1017/s0033291716003469 · Cited by 47
“Studies using electroencephalogram (EEG) (Butler et al. 2007; Boutros et al. 2008), functional MRI (fMRI) (Jones, 1997; Woodward et al.”
MethodClementz, B. A., Wang, J., & Keil, A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4095-08.2008 · Cited by 44
“A host of previous studies suggest that visual processing deficits observed in schizophrenia are not associated with antipsychotic medication treatments (for a brief discussion, see Butler et al., 2007).”
BackgroundAuditory ERP components before and after transition to a first psychotic episode
van Tricht, M. J., Nieman, D. H., Koelman, J. H. T. M., Bour, L. J., van der Meer, J. N., van Amelsvoort, T., LINSZEN, D. H., & de Haan, L. (2011) · Biological Psychology · doi:10.1016/j.biopsycho.2011.04.005 · Cited by 43
Coleman, M. J., Cestnick, L., Krastoshevsky, O., Krause, V., Huang, Z., Mendell, N. R., & Levy, D. L. (2009) · Schizophrenia Bulletin · doi:10.1093/schbul/sbp090 · Cited by 43
Retinal ganglion cells dysfunctions in schizophrenia patients with or without visual hallucinations
Bernardin, F., Schwitzer, T., Angioï-Duprez, K., Giersch, A., Jansen, C., Schwan, R., & Laprévote, V. (2019) · Schizophrenia Research · doi:10.1016/j.schres.2019.07.007 · Cited by 42
Koychev, I. G., McMullen, K., Lees, J., Dadhiwala, R., Grayson, L., Perry, C., Schmechtig, A., Walters, J., Craig, K. J., Dawson, G. R., et al. (2011) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2011.10.005 · Cited by 42
“Also, ample evidence has now accumulated pointing out abnormalities in the earliest stages of information processing that in turn drive higher-order cognitive impairment (Butler et al., 2007; Haenschel et al., 2007).”
Backgroundde Jong, J. J., Hodiamont, P. P. G., & de Gelder, B. (2010) · Schizophrenia Research · doi:10.1016/j.schres.2010.04.010 · Cited by 39
“Early visual dysfunction, including impairments in magnocellular/parvocellular interactions, is also reported in schizophrenia (Butler et al., 2003; Butler et al., 2007).”
BackgroundSchizophrenia and visual backward masking: a general deficit of target enhancement
Herzog, M. H., Roinishvili, M., Chkonia, E. D., & Brand, A. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00254 · Cited by 40
“Enhanced masking in schizophrenic patients is attributed to either a hyperactive or hypoactive magno-cellular visual system (e.g., Green et al., 1994a,b; Schechter et al., 2003; Slaghuis, 2004; Butler et al., 2007).”
BackgroundNeuhaus, A. H., Popescu, F. C., Grozea, C., Hahn, E. W., Hahn, C., Opgen‐Rhein, C., Urbanek, C., & Dettling, M. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.12.038 · Cited by 39
“More generally, this result argues in favor of an early visual processing deficit in schizophrenia and is thus in good accordancewith results from previous studies suggesting similar deficits (Yeap et al., 2006; Butler et al., 2007; Haenschel et al., 2007; Sehatpour et al., 2010).”
BackgroundResultImpaired conscious access and abnormal attentional amplification in schizophrenia
Berkovitch, L., Cul, A. D., Maheu, M., & Dehaene, S. (2018) · NeuroImage Clinical · doi:10.1016/j.nicl.2018.03.010 · Cited by 43
“To account for those results, a specific dysfunction of the magnocellular pathway was hypothesized, while the parvocellular visual pathway was thought to be preserved (Butler et al., 2007, 2005; Javitt, 2009a; Kim et al., 2006; Martínez et al., 2012).”
InfluentialLaprévote, V., Oliva, A., Delerue, C., Thomas, P., & Boucart, M. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2010.10.017 · Cited by 39
“Butler et al. (2007) have measured VEP with sinusoidal gratings and have shown a delayed P1 for LSF but not for HSF.”
Visual sensory processing deficits in schizophrenia: Is there anything to the magnocellular account?
Lalor, E. C., Sanctis, P. D., KRAKOWSKI, M. I., & Foxe, J. J. (2012) · Schizophrenia Research · doi:10.1016/j.schres.2012.05.022 · Cited by 39
“It would also explain why, in Butler et al. (2007), the reduced P1 component preceded the retinotopic, intact C1 component, as reports from monkey studies have suggested that fast activation of dorsal areas such as the middle temporal visual area may occur even before activation of layer 4 of V1 in…”
InfluentialSelf-citationSocial appraisal in chronic psychosis: Role of medial frontal and occipital networks
Taylor, S. F., Chen, A. C., Tso, I. F., Liberzon, I., & Welsh, R. C. (2010) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2010.08.004 · Cited by 39
“These associations may reflect the lack of appropriate top-down influence on early cortical processing, or they may reflect a primary deficit of cortical circuitry, as has been suggested by some groups (Butler et al., 2007).”
Association between failures in perceptual updating and the severity of psychosis in schizophrenia
Bansal, S., Bae, G.-Y., Robinson, B. M., Hahn, B., Waltz, J., Erickson, M., Leptourgos, P., Corlett, P., Luck, S. J., & Gold, J. M. (2022) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2021.3482 · Cited by 35
Robol, V., Tibber, M. S., Anderson, E. J., Bobin, T., Carlin, P., Shergill, S. S., & Dakin, S. C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0060951 · Cited by 37
“compared to high spatial frequency (SF) gratings (for review see [2,3]), a finding that is mirrored in patients exhibiting noisier visual evoked potentials (VEPs) in response to low SF stimuli [4,5].”
Hansen, B. C., Johnson, A. P., & Dave Ellemberg, A. (2012) · Journal of Neurophysiology · doi:10.1152/jn.00288.2012 · Cited by 37
“…configurations (alternating in luminance or color contrast) to spatially complex check or checkerboard patterns (also alternating in luminance or color contrast) to human face stimuli (e.g., Baseler and Sutter 1997; Butler et al. 2007; Foxe et al. 2008; Mitsudo et al. 2011; Schechter et al. 2005).”
BackgroundLencer, R., Keedy, S., Reilly, J. L., McDonough, B. E., Harris, M. S. H., Sprenger, A., & Sweeney, J. A. (2011) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2011.06.011 · Cited by 37
“However, EEG and fMRI studies using alternating gradients rather than motion stimuli have shown reduced responsivity also in primary visual cortex, which we did not observe (Butler et al., 2007; Martinez et al., 2008).”
Cortical thickness, neuron density and size in the inferior parietal lobe in schizophrenia
Smiley, J. F., Konnova, K., & Bleiwas, C. (2012) · Schizophrenia Research · doi:10.1016/j.schres.2012.01.006 · Cited by 35
“This disruption may be partially caused by pathology in subcortical and early cortical sensory pathways (Butler et al., 2007; Martinez et al., 2008), but there is also evidence of pathology in cortical association areas that are sites of multisensory integration.”
BackgroundWang, J., Brown, R., Dobkins, K. R., McDowell, J. E., & Clementz, B. A. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp243 · Cited by 35
Romero, Y. R., KEIL, J. E., Balz, J., Niedeggen, M., Gallinat, J., & Senkowski, D. (2016) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2016.00041 · Cited by 33
“ORIGINAL RESEARCH published: 12 February 2016 doi: 10.3389/fnhum.2016.00041 Edited by: Tetsuo Kida, National Institute for Physiological Sciences, Japan Reviewed by: Pierre Mégevand, Geneva University Hospitals, Switzerland Anne Giersch, Institut National de la Santé et de la Recherche Médicale , France *Correspondenc…”
BackgroundMethodInfluentialKelemen, O., Kovács, T., & Kéri, S. (2013) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2013.06.017 · Cited by 33
Kim, D.-W., Shim, M., Song, M. J., Im, C., & Lee, S. (2014) · Schizophrenia Research · doi:10.1016/j.schres.2014.12.020 · Cited by 34
“recognition in schizophrenia is due to impaired bottom-up processing at a relatively early stage rather than a top-down dysfunction (Butler et al., 2007).”
BackgroundSelf-citationA modality‐specific dysfunction of pain processing in schizophrenia
Zhou, L., Bi, Y., Liang, M., Kong, Y., Tu, Y., Zhang, X., Song, Y., Du, X., Tan, S., & Hu, L. (2019) · Human Brain Mapping · doi:10.1002/hbm.24906 · Cited by 33
“…consequent upon a general deficit of sensory information processing (Javitt & Freedman, 2015), which has been frequently reported in multiple sensory modalities (e.g., auditory, somatosensory, visual) (Braff, Light, & Swerdlow, 2007; Butler et al., 2007; Levy et al., 2000; Turetsky et al., 2008).”
BackgroundWhen and where is binocular rivalry resolved in the visual cortex?
Pitts, M. A., Martı́nez, A., & Hillyard, S. A. (2010) · Journal of Vision · doi:10.1167/10.14.25 · Cited by 34
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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