The impact of visual dysfunctions in recent-onset psychosis and clinical high-risk state for psychosis

the PRONIA consortium; Johanna M. Schwarzer; Inga Meyhoefer; Linda A. Antonucci; Lana Kambeitz-Ilankovic; Marian Surmann; Olga Bienek; Georg Romer; Udo Dannlowski; Tim Hahn; Alexandra Korda; Dominic B. Dwyer; Anne Ruef; Shalaila S. Haas; Marlene Rosen; Theresa Lichtenstein; Stephan Ruhrmann; Joseph Kambeitz; Raimo K.R. Salokangas; Christos Pantelis; Frauke Schultze-Lutter; Eva Meisenzahl; Paolo Brambilla; Alessandro Bertolino; Stefan Borgwardt; Rachel Upthegrove; Nikolaos Koutsouleris; Rebekka Lencer; Maria Fernanda Urquijo

doi:10.1038/s41386-022-01385-3

The impact of visual dysfunctions in recent-onset psychosis and clinical high-risk state for psychosis

the PRONIA consortium, Johanna M. Schwarzer, Inga Meyhoefer, Linda A. Antonucci, Lana Kambeitz-Ilankovic, Marian Surmann, Olga Bienek, Georg Romer, Udo Dannlowski, Tim Hahn, Alexandra Korda, Dominic B. Dwyer, Anne Ruef, Shalaila S. Haas, Marlene Rosen, Theresa Lichtenstein, Stephan Ruhrmann, Joseph Kambeitz, Raimo K.R. Salokangas, Christos PantelisFrauke Schultze-Lutter, Eva Meisenzahl, Paolo Brambilla, Alessandro Bertolino, Stefan Borgwardt, Rachel Upthegrove, Nikolaos Koutsouleris, Rebekka Lencer^*, Maria Fernanda Urquijo

^*Corresponding author for this work

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Abstract

Subtle subjective visual dysfunctions (VisDys) are reported by about 50% of patients with schizophrenia and are suggested to predict psychosis states. Deeper insight into VisDys, particularly in early psychosis states, could foster the understanding of basic disease mechanisms mediating susceptibility to psychosis, and thereby inform preventive interventions. We systematically investigated the relationship between VisDys and core clinical measures across three early phase psychiatric conditions. Second, we used a novel multivariate pattern analysis approach to predict VisDys by resting-state functional connectivity within relevant brain systems. VisDys assessed with the Schizophrenia Proneness Instrument (SPI-A), clinical measures, and resting-state fMRI data were examined in recent-onset psychosis (ROP, n = 147), clinical high-risk states of psychosis (CHR, n = 143), recent-onset depression (ROD, n = 151), and healthy controls (HC, n = 280). Our multivariate pattern analysis approach used pairwise functional connectivity within occipital (ON) and frontoparietal (FPN) networks implicated in visual information processing to predict VisDys. VisDys were reported more often in ROP (50.34%), and CHR (55.94%) than in ROD (16.56%), and HC (4.28%). Higher severity of VisDys was associated with less functional remission in both CHR and ROP, and, in CHR specifically, lower quality of life (Qol), higher depressiveness, and more severe impairment of visuospatial constructability. ON functional connectivity predicted presence of VisDys in ROP (balanced accuracy 60.17%, p = 0.0001) and CHR (67.38%, p = 0.029), while in the combined ROP + CHR sample VisDys were predicted by FPN (61.11%, p = 0.006). These large-sample study findings suggest that VisDys are clinically highly relevant not only in ROP but especially in CHR, being closely related to aspects of functional outcome, depressiveness, and Qol. Findings from multivariate pattern analysis support a model of functional integrity within ON and FPN driving the VisDys phenomenon and being implicated in core disease mechanisms of early psychosis states.

Original language	English
Pages (from-to)	2051-2060
Number of pages	10
Journal	Neuropsychopharmacology
Volume	47
Issue number	12
Early online date	18 Aug 2022
DOIs	https://doi.org/10.1038/s41386-022-01385-3
Publication status	Published - Nov 2022

Bibliographical note

Funding Information:
The presented work was supported by the grant for the Personalized Prognostic Indicators for early Psychosis management (PRONIA Study): EU-FP7-HEALTH; agreement number: 602152. LK-I is a recipient of an NARSAD Young Investigator Award of the Brain & Behavior Research Foundation No. 28474. TL was additionally supported by the Koeln Fortune Program/Faculty of Medicine, University of Cologne. RL received additional funding from the European Unions Horizon 2020 research and innovation program under the Marie Sklodowska-Curie grant agreement No. 734227. Open Access funding enabled and organized by Projekt DEAL.

RU reports grants from the Medical Research Council, National Institute for Health Research: Health Technology Assessment, the National Institute of Mental Health, and personal fees from Sunovion, Springer Heathcare and Vitaris outside the submitted work. TL reports funding from Koeln Fortune Program/Faculty of Medicine, University of Cologne (No 370/2020) outside the submitted work. RL participated in advisory boards and received honoraria for talks presented at educational meetings organized by Janssen-Cilag, Otsuka/Lundbeck and ROVI outside the submitted work. No other conflicts of interest were reported.

Publisher Copyright:
© 2022, The Author(s).

Keywords

Brain/diagnostic imaging
Humans
Magnetic Resonance Imaging
Psychotic Disorders
Quality of Life
Schizophrenia

ASJC Scopus subject areas

Psychiatry and Mental health
Pharmacology

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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SchwarzerJ2022impactFinal published version, 2.07 MBLicence: Creative Commons: Attribution (CC BY)

FP7_COLLAB - PRONIA
Upthegrove, R.
European Commission - Management Costs, European Commission
1/10/13 → 31/03/19
Project: Research

Cite this

the PRONIA consortium, Schwarzer, J. M., Meyhoefer, I., Antonucci, L. A., Kambeitz-Ilankovic, L., Surmann, M., Bienek, O., Romer, G., Dannlowski, U., Hahn, T., Korda, A., Dwyer, D. B., Ruef, A., Haas, S. S., Rosen, M., Lichtenstein, T., Ruhrmann, S., Kambeitz, J., Salokangas, R. K. R., ... Urquijo, M. F. (2022). The impact of visual dysfunctions in recent-onset psychosis and clinical high-risk state for psychosis. Neuropsychopharmacology, 47(12), 2051-2060. https://doi.org/10.1038/s41386-022-01385-3

@article{04520cd4bbd14281ba730f4e3d7a71d5,

title = "The impact of visual dysfunctions in recent-onset psychosis and clinical high-risk state for psychosis",

abstract = "Subtle subjective visual dysfunctions (VisDys) are reported by about 50% of patients with schizophrenia and are suggested to predict psychosis states. Deeper insight into VisDys, particularly in early psychosis states, could foster the understanding of basic disease mechanisms mediating susceptibility to psychosis, and thereby inform preventive interventions. We systematically investigated the relationship between VisDys and core clinical measures across three early phase psychiatric conditions. Second, we used a novel multivariate pattern analysis approach to predict VisDys by resting-state functional connectivity within relevant brain systems. VisDys assessed with the Schizophrenia Proneness Instrument (SPI-A), clinical measures, and resting-state fMRI data were examined in recent-onset psychosis (ROP, n = 147), clinical high-risk states of psychosis (CHR, n = 143), recent-onset depression (ROD, n = 151), and healthy controls (HC, n = 280). Our multivariate pattern analysis approach used pairwise functional connectivity within occipital (ON) and frontoparietal (FPN) networks implicated in visual information processing to predict VisDys. VisDys were reported more often in ROP (50.34%), and CHR (55.94%) than in ROD (16.56%), and HC (4.28%). Higher severity of VisDys was associated with less functional remission in both CHR and ROP, and, in CHR specifically, lower quality of life (Qol), higher depressiveness, and more severe impairment of visuospatial constructability. ON functional connectivity predicted presence of VisDys in ROP (balanced accuracy 60.17%, p = 0.0001) and CHR (67.38%, p = 0.029), while in the combined ROP + CHR sample VisDys were predicted by FPN (61.11%, p = 0.006). These large-sample study findings suggest that VisDys are clinically highly relevant not only in ROP but especially in CHR, being closely related to aspects of functional outcome, depressiveness, and Qol. Findings from multivariate pattern analysis support a model of functional integrity within ON and FPN driving the VisDys phenomenon and being implicated in core disease mechanisms of early psychosis states.",

keywords = "Brain/diagnostic imaging, Humans, Magnetic Resonance Imaging, Psychotic Disorders, Quality of Life, Schizophrenia",

author = "{the PRONIA consortium} and Schwarzer, {Johanna M.} and Inga Meyhoefer and Antonucci, {Linda A.} and Lana Kambeitz-Ilankovic and Marian Surmann and Olga Bienek and Georg Romer and Udo Dannlowski and Tim Hahn and Alexandra Korda and Dwyer, {Dominic B.} and Anne Ruef and Haas, {Shalaila S.} and Marlene Rosen and Theresa Lichtenstein and Stephan Ruhrmann and Joseph Kambeitz and Salokangas, {Raimo K.R.} and Christos Pantelis and Frauke Schultze-Lutter and Eva Meisenzahl and Paolo Brambilla and Alessandro Bertolino and Stefan Borgwardt and Rachel Upthegrove and Nikolaos Koutsouleris and Rebekka Lencer and Alkomiet Hasan and Claudius Hoff and Ifrah Khanyaree and Aylin Melo and Susanna Muckenhuber-Sternbauer and Yanis K{\"o}hler and {\"O}mer {\"O}zt{\"u}rk and Nora Penzel and David Popovic and Adrian Rangnick and {von Saldern}, Sebastian and Rachele Sanfelici and Moritz Spangemacher and Ana Tupac and Urquijo, {Maria Fernanda} and Johanna Weiske and Griffiths, {Sian Lowri} and Mariam Iqbal and Mirabel Pelton and Pavan Mallikarjun and Alexandra Stainton and Ashleigh Lin and Paris Lalousis",

note = "Funding Information: The presented work was supported by the grant for the Personalized Prognostic Indicators for early Psychosis management (PRONIA Study): EU-FP7-HEALTH; agreement number: 602152. LK-I is a recipient of an NARSAD Young Investigator Award of the Brain & Behavior Research Foundation No. 28474. TL was additionally supported by the Koeln Fortune Program/Faculty of Medicine, University of Cologne. RL received additional funding from the European Unions Horizon 2020 research and innovation program under the Marie Sklodowska-Curie grant agreement No. 734227. Open Access funding enabled and organized by Projekt DEAL. RU reports grants from the Medical Research Council, National Institute for Health Research: Health Technology Assessment, the National Institute of Mental Health, and personal fees from Sunovion, Springer Heathcare and Vitaris outside the submitted work. TL reports funding from Koeln Fortune Program/Faculty of Medicine, University of Cologne (No 370/2020) outside the submitted work. RL participated in advisory boards and received honoraria for talks presented at educational meetings organized by Janssen-Cilag, Otsuka/Lundbeck and ROVI outside the submitted work. No other conflicts of interest were reported. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

year = "2022",

month = nov,

doi = "10.1038/s41386-022-01385-3",

language = "English",

volume = "47",

pages = "2051--2060",

journal = "Neuropsychopharmacology",

issn = "0893-133X",

publisher = "Nature Publishing Group",

number = "12",

}

the PRONIA consortium, Schwarzer, JM, Meyhoefer, I, Antonucci, LA, Kambeitz-Ilankovic, L, Surmann, M, Bienek, O, Romer, G, Dannlowski, U, Hahn, T, Korda, A, Dwyer, DB, Ruef, A, Haas, SS, Rosen, M, Lichtenstein, T, Ruhrmann, S, Kambeitz, J, Salokangas, RKR, Pantelis, C, Schultze-Lutter, F, Meisenzahl, E, Brambilla, P, Bertolino, A, Borgwardt, S, Upthegrove, R, Koutsouleris, N, Lencer, R & Urquijo, MF 2022, 'The impact of visual dysfunctions in recent-onset psychosis and clinical high-risk state for psychosis', Neuropsychopharmacology, vol. 47, no. 12, pp. 2051-2060. https://doi.org/10.1038/s41386-022-01385-3

TY - JOUR

T1 - The impact of visual dysfunctions in recent-onset psychosis and clinical high-risk state for psychosis

AU - the PRONIA consortium

AU - Schwarzer, Johanna M.

AU - Meyhoefer, Inga

AU - Antonucci, Linda A.

AU - Kambeitz-Ilankovic, Lana

AU - Surmann, Marian

AU - Bienek, Olga

AU - Romer, Georg

AU - Dannlowski, Udo

AU - Hahn, Tim

AU - Korda, Alexandra

AU - Dwyer, Dominic B.

AU - Ruef, Anne

AU - Haas, Shalaila S.

AU - Rosen, Marlene

AU - Lichtenstein, Theresa

AU - Ruhrmann, Stephan

AU - Kambeitz, Joseph

AU - Salokangas, Raimo K.R.

AU - Pantelis, Christos

AU - Schultze-Lutter, Frauke

AU - Meisenzahl, Eva

AU - Brambilla, Paolo

AU - Bertolino, Alessandro

AU - Borgwardt, Stefan

AU - Upthegrove, Rachel

AU - Koutsouleris, Nikolaos

AU - Lencer, Rebekka

AU - Hasan, Alkomiet

AU - Hoff, Claudius

AU - Khanyaree, Ifrah

AU - Melo, Aylin

AU - Muckenhuber-Sternbauer, Susanna

AU - Köhler, Yanis

AU - Öztürk, Ömer

AU - Penzel, Nora

AU - Popovic, David

AU - Rangnick, Adrian

AU - von Saldern, Sebastian

AU - Sanfelici, Rachele

AU - Spangemacher, Moritz

AU - Tupac, Ana

AU - Urquijo, Maria Fernanda

AU - Weiske, Johanna

AU - Griffiths, Sian Lowri

AU - Iqbal, Mariam

AU - Pelton, Mirabel

AU - Mallikarjun, Pavan

AU - Stainton, Alexandra

AU - Lin, Ashleigh

AU - Lalousis, Paris

N1 - Funding Information: The presented work was supported by the grant for the Personalized Prognostic Indicators for early Psychosis management (PRONIA Study): EU-FP7-HEALTH; agreement number: 602152. LK-I is a recipient of an NARSAD Young Investigator Award of the Brain & Behavior Research Foundation No. 28474. TL was additionally supported by the Koeln Fortune Program/Faculty of Medicine, University of Cologne. RL received additional funding from the European Unions Horizon 2020 research and innovation program under the Marie Sklodowska-Curie grant agreement No. 734227. Open Access funding enabled and organized by Projekt DEAL. RU reports grants from the Medical Research Council, National Institute for Health Research: Health Technology Assessment, the National Institute of Mental Health, and personal fees from Sunovion, Springer Heathcare and Vitaris outside the submitted work. TL reports funding from Koeln Fortune Program/Faculty of Medicine, University of Cologne (No 370/2020) outside the submitted work. RL participated in advisory boards and received honoraria for talks presented at educational meetings organized by Janssen-Cilag, Otsuka/Lundbeck and ROVI outside the submitted work. No other conflicts of interest were reported. Publisher Copyright: © 2022, The Author(s).

PY - 2022/11

Y1 - 2022/11

N2 - Subtle subjective visual dysfunctions (VisDys) are reported by about 50% of patients with schizophrenia and are suggested to predict psychosis states. Deeper insight into VisDys, particularly in early psychosis states, could foster the understanding of basic disease mechanisms mediating susceptibility to psychosis, and thereby inform preventive interventions. We systematically investigated the relationship between VisDys and core clinical measures across three early phase psychiatric conditions. Second, we used a novel multivariate pattern analysis approach to predict VisDys by resting-state functional connectivity within relevant brain systems. VisDys assessed with the Schizophrenia Proneness Instrument (SPI-A), clinical measures, and resting-state fMRI data were examined in recent-onset psychosis (ROP, n = 147), clinical high-risk states of psychosis (CHR, n = 143), recent-onset depression (ROD, n = 151), and healthy controls (HC, n = 280). Our multivariate pattern analysis approach used pairwise functional connectivity within occipital (ON) and frontoparietal (FPN) networks implicated in visual information processing to predict VisDys. VisDys were reported more often in ROP (50.34%), and CHR (55.94%) than in ROD (16.56%), and HC (4.28%). Higher severity of VisDys was associated with less functional remission in both CHR and ROP, and, in CHR specifically, lower quality of life (Qol), higher depressiveness, and more severe impairment of visuospatial constructability. ON functional connectivity predicted presence of VisDys in ROP (balanced accuracy 60.17%, p = 0.0001) and CHR (67.38%, p = 0.029), while in the combined ROP + CHR sample VisDys were predicted by FPN (61.11%, p = 0.006). These large-sample study findings suggest that VisDys are clinically highly relevant not only in ROP but especially in CHR, being closely related to aspects of functional outcome, depressiveness, and Qol. Findings from multivariate pattern analysis support a model of functional integrity within ON and FPN driving the VisDys phenomenon and being implicated in core disease mechanisms of early psychosis states.

AB - Subtle subjective visual dysfunctions (VisDys) are reported by about 50% of patients with schizophrenia and are suggested to predict psychosis states. Deeper insight into VisDys, particularly in early psychosis states, could foster the understanding of basic disease mechanisms mediating susceptibility to psychosis, and thereby inform preventive interventions. We systematically investigated the relationship between VisDys and core clinical measures across three early phase psychiatric conditions. Second, we used a novel multivariate pattern analysis approach to predict VisDys by resting-state functional connectivity within relevant brain systems. VisDys assessed with the Schizophrenia Proneness Instrument (SPI-A), clinical measures, and resting-state fMRI data were examined in recent-onset psychosis (ROP, n = 147), clinical high-risk states of psychosis (CHR, n = 143), recent-onset depression (ROD, n = 151), and healthy controls (HC, n = 280). Our multivariate pattern analysis approach used pairwise functional connectivity within occipital (ON) and frontoparietal (FPN) networks implicated in visual information processing to predict VisDys. VisDys were reported more often in ROP (50.34%), and CHR (55.94%) than in ROD (16.56%), and HC (4.28%). Higher severity of VisDys was associated with less functional remission in both CHR and ROP, and, in CHR specifically, lower quality of life (Qol), higher depressiveness, and more severe impairment of visuospatial constructability. ON functional connectivity predicted presence of VisDys in ROP (balanced accuracy 60.17%, p = 0.0001) and CHR (67.38%, p = 0.029), while in the combined ROP + CHR sample VisDys were predicted by FPN (61.11%, p = 0.006). These large-sample study findings suggest that VisDys are clinically highly relevant not only in ROP but especially in CHR, being closely related to aspects of functional outcome, depressiveness, and Qol. Findings from multivariate pattern analysis support a model of functional integrity within ON and FPN driving the VisDys phenomenon and being implicated in core disease mechanisms of early psychosis states.

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KW - Humans

KW - Magnetic Resonance Imaging

KW - Psychotic Disorders

KW - Quality of Life

KW - Schizophrenia

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SN - 0893-133X

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SP - 2051

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JO - Neuropsychopharmacology

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IS - 12

ER -

The impact of visual dysfunctions in recent-onset psychosis and clinical high-risk state for psychosis

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

UN SDGs

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Projects

FP7_COLLAB - PRONIA

Cite this