Impaired prefrontal synaptic gain in people with psychosis and their relatives during the mismatch negativity
Open accessAbstract
The mismatch negativity (MMN) evoked potential, a preattentive brain response to a discriminable change in auditory stimulation, is significantly reduced in psychosis. Glutamatergic theories of psychosis propose that hypofunction of NMDA receptors (on pyramidal cells and inhibitory interneurons) causes a loss of synaptic gain control. We measured changes in neuronal effective connectivity underlying the MMN using dynamic causal modeling (DCM), where the gain (excitability) of superficial pyramidal cells is explicitly parameterised. EEG data were obtained during a MMN task--for 24 patients with psychosis, 25 of their first-degree unaffected relatives, and 35 controls--and DCM was used to estimate the excitability (modeled as self-inhibition) of (source-specific) superficial pyramidal populations. The MMN sources, based on previous research, included primary and secondary auditory cortices, and the right inferior frontal gyrus. Both patients with psychosis and unaffected relatives (to a lesser degree) showed increased excitability in right inferior frontal gyrus across task conditions, compared to controls. Furthermore, in the same region, both patients and their relatives showed a reversal of the normal response to deviant stimuli; that is, a decrease in excitability in comparison to standard conditions. Our results suggest that psychosis and genetic risk for the illness are associated with both context-dependent (condition-specific) and context-independent abnormalities of the excitability of superficial pyramidal cell populations in the MMN paradigm. These abnormalities could relate to NMDA receptor hypofunction on both pyramidal cells and inhibitory interneurons, and appear to be linked to the genetic aetiology of the illness, thereby constituting potential endophenotypes for psychosis.
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Within the DCM framework, decreased self-inhibition represents an increase in excitability and an overweighting of sensory prediction errors.
“Within the DCM framework, decreased self-inhibition represents an increase in excitability and an overweighting of sensory prediction errors24,46.”
From Deviations in effective connectivity explain different hallucination subtypes in Parkinson's disease psychosis (2026) · cites this paper as [46]
Ranlund et al. found significant differences in the intrinsic connections of the right IFG among patients with psychosis, unaffected relatives, and healthy individuals.
“They found significant differences in the intrinsic connections of the right IFG among patients with psychosis, unaffected relatives, and healthy individuals.”
From A Predictive Coding Perspective on Mismatch Negativity Impairment in Schizophrenia (2020) · cites this paper as [44]
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Müller, B. W., Jüptner, M., Jentzen, W., & Müller, S. P. (2002) · NeuroImage · doi:10.1006/nimg.2002.1176 · Cited by 112 · see citing works
Modeling ketamine effects on synaptic plasticity during the mismatch negativity
Schmidt, A., Diaconescu, A. O., Kometer, M., Friston, K. J., Stephan, K. E., & Vollenweider, F. X. (2013) · Cerebral Cortex · doi:10.1093/cercor/bhs238 · Cited by 109 · see citing works
Self-citationBaldeweg, T., & Hirsch, S. R. (2015) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2014.03.008 · Cited by 108 · see citing works
Dynamic causal modeling with neural fields
Pinotsis, D. A., Moran, R., & Friston, K. J. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.08.020 · Cited by 101 · see citing works
Self-citationSchmidt, A., Smieskova, R., Aston, J., Simon, A., Allen, P., Fusar-Poli, P., McGuire, P. K., Riecher-Rössler, A., Stephan, K. E., & Borgwardt, S. (2013) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2013.117 · Cited by 93 · see citing works
Näätänen, R., & Kreegipuu, K. (2011) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780195374148.013.0081 · Cited by 92 · see citing works
Quantitative EEG in schizophrenia and in response to acute and chronic clozapine treatment
Knott, V., Labelle, A., Jones, B., & Mahoney, C. (2001) · Schizophrenia Research · doi:10.1016/s0920-9964(00)00165-1 · Cited by 92 · see citing works
Dima, D., Jogia, J., Collier, D. A., Vassos, E., Burdick, K. E., & Frangou, S. (2013) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2013.2099 · Cited by 89 · see citing works
Dietz, M. J., Friston, K. J., Mattingley, J. B., Roepstorff, A., & Garrido, M. I. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.3765-13.2014 · Cited by 86 · see citing works
Self-citationThe functional anatomy of schizophrenia: A dynamic causal modeling study of predictive coding
Fogelson, N., Litvak, V., Peled, A., Fernandez-del-Olmo, M., & Friston, K. (2014) · Schizophrenia Research · doi:10.1016/j.schres.2014.06.011 · Cited by 85 · cited 7× · see citing works
“Several previous DCM studies have found abnormal effective connectivity in psychosis, both using EEG/MEG [Dima et al., 2010, 2012; Fogelson et al., 2014; Roiser et al., 2013] and fMRI methods [Crossley et al.”
MethodInfluentialSelf-citationAuditory P300 in patients with bipolar disorder and their unaffected relatives
Schulze, K. K., Hall, M., McDonald, C., Marshall, N., Walshe, M., Murray, R. M., & Bramon, E. (2008) · Bipolar Disorders · doi:10.1111/j.1399-5618.2007.00527.x · Cited by 82 · see citing works
Self-citationDysconnectivity in the Frontoparietal Attention Network in Schizophrenia
Roiser, J. P., Wigton, R. L., Kilner, J. M., Méndez, M. A., Hon, N., Friston, K. J., & Joyce, E. M. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00176 · Cited by 75 · see citing works
Self-citationPhillips, W. A., & Silverstein, S. M. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00307 · Cited by 75 · see citing works
Dittmann-Balçar, A., Jüptner, M., Jentzen, W., & Schall, U. (2001) · Neuroscience Letters · doi:10.1016/s0304-3940(01)01995-4 · Cited by 73 · see citing works
Resting EEG in psychosis and at-risk populations — A possible endophenotype?
Ranlund, S. M., Nottage, J. F., Shaikh, M., Dutt, A., Constante, M., Walshe, M., Hall, M., Friston, K. J., Murray, R. M., & Bramon, E. (2014) · Schizophrenia Research · doi:10.1016/j.schres.2013.12.017 · Cited by 71 · see citing works
Self-citationContrast gain control and horizontal interactions in V1: A DCM study
Pinotsis, D. A., Brunet, N., Bastos, A., Bosman, C. A., Litvak, V., Fries, P., & Friston, K. J. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.01.047 · Cited by 68 · cited 3× · see citing works
“Given the prominence of NMDA-Rs in superficial cortical layers, it is unsurprising that the gain of superficial pyramidal cell populations is strongly affected by NMDAR function [Fox et al., 1990; Pinotsis et al., 2014].”
BackgroundSelf-citationA New Role for Endophenotypes in the GWAS Era: Functional Characterization of Risk Variants
Hall, M.-H. (2010) · Harvard Review of Psychiatry · doi:10.3109/10673220903523532 · Cited by 66 · cited 2× · see citing works
“The use of endophenotypes might help clarify the functional effects of genetic risk variants identified [Bramon et al., 2014; Hall and Smoller, 2010], and further research could investigate whether deviant-related changes in excitability can predict genotype; for example, looking at candidate genes…”
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Dima, D., Frangou, S., Burge, L., Braeutigam, S., & James, A. C. (2012) · Schizophrenia Research · doi:10.1016/j.schres.2011.12.024 · Cited by 65 · see citing works
Dynamic causal modelling of lateral interactions in the visual cortex
Pinotsis, D. A., Schwarzkopf, D. S., Vladimir Litvak, A., Rees, G. E., Barnes, G. R., & Friston, K. J. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.10.078 · Cited by 64 · see citing works
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Mismatch negativity and low frequency oscillations in schizophrenia families
Hong, L. E., Moran, L. V., Du, X. M., O’Donnell, P., & Summerfelt, A. T. (2012) · Clinical Neurophysiology · doi:10.1016/j.clinph.2012.03.011 · Cited by 61 · see citing works
Mismatch Negativity in Recent-Onset and Chronic Schizophrenia: A Current Source Density Analysis
Fulham, W. R., Michie, P. T., Ward, P. B., Rasser, P. E., Todd, J., Johnston, P., Thompson, P. M., & Schall, U. (2014) · PLoS ONE · doi:10.1371/journal.pone.0100221 · Cited by 56 · see citing works
Bramon, E., Pirinen, M., Strange, A., Lin, K., Freeman, C., Bellenguez, C., Su, Z., Band, G., Pearson, R. D., Vukcevic, D., et al. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.03.033 · Cited by 51 · see citing works
Self-citationKim, M., Kim, S. N., Lee, S., Byun, M. S., Shin, K. S., Park, H. Y., Jang, J. H., & Kwon, J. S. (2014) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2014.02.012 · Cited by 46 · see citing works
Abnormal effective connectivity and psychopathological symptoms in the psychosis high-risk state
Schmidt, A., Smieskova, R., Simon, A. E., Allen, P., Fusar‐Poli, P., McGuire, P. K., Bendfeldt, K., Aston, J., Lang, U. E., Walter, M., et al. (2014) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.130102 · Cited by 46 · see citing works
Diwadkar, V. A., Bakshi, N. K., Gupta, G., Pruitt, P. J., White, R. T., & Eickhoff, S. B. (2014) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2014.00050 · Cited by 46 · see citing works
Matsubayashi, J., Kawakubo, Y., Suga, M., Takei, Y., Kumano, S., Fukuda, M., Itoh, K., Yumoto, M., & Kasai, K. (2008) · Brain Research · doi:10.1016/j.brainres.2008.07.120 · Cited by 44 · see citing works
Tiitinen, H., Salminen, N. H., Palomäki, K. J., Mäkinen, V. T., Alku, P., & May, P. (2005) · Neuroscience Letters · doi:10.1016/j.neulet.2005.11.018 · Cited by 44 · see citing works
Probing GABA Receptor Function in Schizophrenia with Iomazenil
Ahn, K.-H., Gil, R. B., Seibyl, J. P., Sewell, R. A., & D’Souza, D. C. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.198 · Cited by 40 · see citing works
Correction: A Neurocomputational Model of the Mismatch Negativity
Lieder, F., Stephan, K. E., Jean Daunizeau, A., Garrido, M. I., & Friston, K. J. (2013) · PLoS Computational Biology · doi:10.1371/annotation/ca4c3cdf-9573-4a93-9542-3a62cdbb8396 · Cited by 39 · see citing works
Self-citationDynamical causal modelling for M/EEG: Spatial and temporal symmetry constraints
Fastenrath, M., Friston, K. J., & Kiebel, S. J. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.07.041 · Cited by 31 · see citing works
Self-citationA mechanistic model of mismatch negativity in the ageing brain
Cooray, G., Garrido, M. I., Hyllienmark, L., & Brismar, T. (2014) · Clinical Neurophysiology · doi:10.1016/j.clinph.2014.01.015 · Cited by 30 · see citing works
Neuropathology of Schizophrenia
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Frontal gamma noise power and cognitive domains in schizophrenia
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Effect of DISC1 on the P300 Waveform in Psychosis
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Self-citationVerification of the Mismatch Negativity (MMN) responses in normal adult subjects
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Flagged first, then by citations
Research works printed but not linked: 1
- NICE (2014): Psychosis and schizophrenia in adults: Treatment and management. NICE clinical guideline 178. London: National Institute for Health and Care Excellence. 25340235
Cited by
Sorted by citations
Computational nosology and precision psychiatry
Friston, K. J., Redish, A. D., & Gordon, J. A. (2017) · Computational Psychiatry · doi:10.1162/cpsy_a_00001 · Cited by 126 · see citing works
Self-citationAdams, R. A., Pinotsis, D., Tsirlis, K., Unruh, L., Mahajan, A., Horas, A. M., Convertino, L., Summerfelt, A., Sampath, H., Du, X. M., et al. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2021.07.024 · Cited by 98 · see citing works
Self-citationSensory prediction errors in the continuum of psychosis
Randeniya, R., Oestreich, L. K. L., & Garrido, M. I. (2018) · Schizophrenia Research · doi:10.1016/j.schres.2017.04.019 · Cited by 78 · see citing works
Rosch, R. E., Auksztulewicz, R., Leung, P. D., Friston, K. J., & Baldeweg, T. (2019) · Biological Psychiatry: Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2018.07.003 · Cited by 56 · see citing works
Self-citationA Predictive Coding Perspective on Mismatch Negativity Impairment in Schizophrenia
Kirihara, K., Tada, M., Koshiyama, D., Fujioka, M., Usui, K., Araki, T., & Kasai, K. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00660 · Cited by 51 · see citing works
“Ranlund and colleagues applied DCM to EEG data during the classical oddball paradigm (44).”
MethodDzafic, I., Larsen, K. M., Darke, H., Pertile, H., Carter, O., Sundram, S., & Garrido, M. I. (2021) · Schizophrenia Bulletin · doi:10.1093/schbul/sbaa188 · Cited by 24 · see citing works
Transcriptome-wide association study reveals two genes that influence mismatch negativity
Bhat, A., Irizar, H., Thygesen, J. H., Kuchenbaecker, K., Pain, O., Adams, R. A., Zartaloudi, E., Harju-Seppänen, J., Austin-Zimmerman, I., Wang, B., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108868 · Cited by 17 · see citing works
Self-citationVignando, M., Ffytche, D., Mazibuko, N., Palma, G., Bhat, A., Montagnese, M., Dave, S., Tai, Y. F., Batzu, L., Leta, V., et al. (2026) · Nature Mental Health · doi:10.1038/s44220-026-00669-7
“Within the DCM framework, decreased self-inhibition represents an increase in excitability and an overweighting of sensory prediction errors 24,46 .”
- Authors
- Ranlund, S., Adams, R. A., Díez, Á., Constante, M., Dutt, A., Hall, M., Maestro Carbayo, A., McDonald, C., Petrella, S., Schulze, K., Shaikh, M., Walshe, M., Friston, K., Pinotsis, D., & Bramon, E.
- Affiliations
- University College London (GB)
- Department of PsychiatryHospital Beatriz AngeloLisbon Portugal
- King's College London (GB)
- Harvard University (US)
- The South London and Maudsley NHS Foundation TrustNIHR Biomedical Research Centre for Mental Health at the Institute of Psychiatry, Psychology and Neuroscience, King's College London United Kingdom
- Ollscoil na Gaillimhe – University of Galway (IE)
- University of Foggia (IT)
- South London and Maudsley NHS Foundation Trust (GB)
- Wellcome Centre for Human Neuroimaging (GB)
- Corresponding author
- Ranlund, Siri
- ORCID
- Venue
- Human Brain Mapping
- Publisher
- Wiley
- Published
- 2015-10-27
- Volume
- 37
- Issue
- 1
- Pages
- 351-365
- ISSN
- 1065-9471 (ISSN-L)
- 1097-0193
- PMC
- PMC4843949
- OpenAlex
- W2346160145
- Cited by
- 77
- References
- 132
- Citations by year
- 2026: 6 · 2025: 5 · 2024: 7 · 2023: 7 · 2022: 7 · 2021: 8 · 2020: 12 · 2019: 4 · 2018: 8 · 2017: 8 · 2016: 5
- FWCI
- 5.69
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Human Brain Mapping (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- ARAN (University of Galway Research Repository) (Ollscoil na Gaillimhe – University of Galway) (acceptedVersion, cc-by-nc-nd)
- City Research Online (City University London) (acceptedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- Arrow@dit (Dublin Institute of Technology) (submittedVersion)
- ARAN (University of Galway Research Repository) (Ollscoil na Gaillimhe – University of Galway) (submittedVersion, cc-by-nc-nd)
- UCL Discovery (University College London) (submittedVersion)
- University of Galway Research Repository (submittedVersion, cc-by-nc)
- UVaDOC UVaDOC University of Valladolid Documentary Repository (University of Valladolid) (submittedVersion, other-oa)
- Research Repository UCD (University College Dublin) (cc-by-nc)
- Funders
- National Institute for Health Research, UK (PDA/02/06/016)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Keywords
- psychosis, mismatch negativity, NMDA receptor hypofunction, pyramidal neurons, inhibitory interneurons, dynamic causal modeling, first-degree relatives, genetic risk, endophenotypes, inferior frontal gyrus, auditory cortex
- MeSH terms
- Acoustic Stimulation, Adolescent, Adult, Brain Injuries, Contingent Negative Variation, Electroencephalography, Evoked Potentials, Auditory, Family, Female, Humans, Male, Middle Aged, Models, Theoretical, Psychotic Disorders, Prefrontal Cortex, Nonlinear Dynamics, Young Adult
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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