Virtual Ontogeny of Cortical Growth Preceding Mental Illness

Yash Patel; Jean Shin; Christoph Abé; Ingrid Agartz; Clara Alloza; Dag Alnæs; Sonia Ambrogi; Linda A Antonucci; Celso Arango; Volker Arolt; Guillaume Auzias; Rosa Ayesa-Arriola; Nerisa Banaj; Tobias Banaschewski; Cibele Bandeira; Zeynep Başgöze; Renata Basso Cupertino; Claiton H D Bau; Jochen Bauer; Sarah Baumeister; Fabio Bernardoni; Alessandro Bertolino; Caterina Del Mar Bonnin; Daniel Brandeis; Silvia Brem; Jason Bruggemann; Robin Bülow; Juan R Bustillo; Sara Calderoni; Rosa Calvo; Erick J Canales-Rodríguez; Dara M Cannon; Susanna Carmona; Vaughan J Carr; Stanley V Catts; Sneha Chenji; Qian Hui Chew; David Coghill; Colm G Connolly; Annette Conzelmann; Alexander R Craven; Benedicto Crespo-Facorro; Kathryn Cullen; Andreas Dahl; Udo Dannlowski; Christopher G Davey; Christine Deruelle; Covadonga M Díaz-Caneja; Katharina Dohm; David Willinger

doi:10.1016/j.biopsych.2022.02.959

Virtual Ontogeny of Cortical Growth Preceding Mental Illness

Yash Patel, Jean Shin, Christoph Abé, Ingrid Agartz, Clara Alloza, Dag Alnæs, Sonia Ambrogi, Linda A Antonucci, Celso Arango, Volker Arolt, Guillaume Auzias, Rosa Ayesa-Arriola, Nerisa Banaj, Tobias Banaschewski, Cibele Bandeira, Zeynep Başgöze, Renata Basso Cupertino, Claiton H D Bau, Jochen Bauer, Sarah BaumeisterFabio Bernardoni, Alessandro Bertolino, Caterina Del Mar Bonnin, Daniel Brandeis, Silvia Brem, Jason Bruggemann, Robin Bülow, Juan R Bustillo, Sara Calderoni, Rosa Calvo, Erick J Canales-Rodríguez, Dara M Cannon, Susanna Carmona, Vaughan J Carr, Stanley V Catts, Sneha Chenji, Qian Hui Chew, David Coghill, Colm G Connolly, Annette Conzelmann, Alexander R Craven, Benedicto Crespo-Facorro, Kathryn Cullen, Andreas Dahl, Udo Dannlowski, Christopher G Davey, Christine Deruelle, Covadonga M Díaz-Caneja, Katharina Dohm, David Willinger

Research output: Journal article (peer-reviewed) › Journal article

15 Citations (Scopus)

Abstract

BACKGROUND: Morphology of the human cerebral cortex differs across psychiatric disorders, with neurobiology and developmental origins mostly undetermined. Deviations in the tangential growth of the cerebral cortex during pre/perinatal periods may be reflected in individual variations in cortical surface area later in life.

METHODS: Interregional profiles of group differences in surface area between cases and controls were generated using T1-weighted magnetic resonance imaging from 27,359 individuals including those with attention-deficit/hyperactivity disorder, autism spectrum disorder, bipolar disorder, major depressive disorder, schizophrenia, and high general psychopathology (through the Child Behavior Checklist). Similarity of interregional profiles of group differences in surface area and prenatal cell-specific gene expression was assessed.

RESULTS: Across the 11 cortical regions, group differences in cortical area for attention-deficit/hyperactivity disorder, schizophrenia, and Child Behavior Checklist were dominant in multimodal association cortices. The same interregional profiles were also associated with interregional profiles of (prenatal) gene expression specific to proliferative cells, namely radial glia and intermediate progenitor cells (greater expression, larger difference), as well as differentiated cells, namely excitatory neurons and endothelial and mural cells (greater expression, smaller difference). Finally, these cell types were implicated in known pre/perinatal risk factors for psychosis. Genes coexpressed with radial glia were enriched with genes implicated in congenital abnormalities, birth weight, hypoxia, and starvation. Genes coexpressed with endothelial and mural genes were enriched with genes associated with maternal hypertension and preterm birth.

CONCLUSIONS: Our findings support a neurodevelopmental model of vulnerability to mental illness whereby prenatal risk factors acting through cell-specific processes lead to deviations from typical brain development during pregnancy.

Original language	English
Pages (from-to)	299-313
Number of pages	15
Journal	Biological Psychiatry
Volume	92
Issue number	4
DOIs	https://doi.org/10.1016/j.biopsych.2022.02.959
Publication status	Published - 15 Aug 2022
Externally published	Yes

Keywords

Attention Deficit Disorder with Hyperactivity
Autism Spectrum Disorder/genetics
Bipolar Disorder
Cerebral Cortex
Child
Depressive Disorder, Major/pathology
Female
Humans
Infant, Newborn
Magnetic Resonance Imaging/methods
Pregnancy
Premature Birth/pathology

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10.1016/j.biopsych.2022.02.959

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Patel, Y., Shin, J., Abé, C., Agartz, I., Alloza, C., Alnæs, D., Ambrogi, S., Antonucci, L. A., Arango, C., Arolt, V., Auzias, G., Ayesa-Arriola, R., Banaj, N., Banaschewski, T., Bandeira, C., Başgöze, Z., Cupertino, R. B., Bau, C. H. D., Bauer, J., ... Willinger, D. (2022). Virtual Ontogeny of Cortical Growth Preceding Mental Illness. Biological Psychiatry, 92(4), 299-313. https://doi.org/10.1016/j.biopsych.2022.02.959

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title = "Virtual Ontogeny of Cortical Growth Preceding Mental Illness",

abstract = "BACKGROUND: Morphology of the human cerebral cortex differs across psychiatric disorders, with neurobiology and developmental origins mostly undetermined. Deviations in the tangential growth of the cerebral cortex during pre/perinatal periods may be reflected in individual variations in cortical surface area later in life.METHODS: Interregional profiles of group differences in surface area between cases and controls were generated using T1-weighted magnetic resonance imaging from 27,359 individuals including those with attention-deficit/hyperactivity disorder, autism spectrum disorder, bipolar disorder, major depressive disorder, schizophrenia, and high general psychopathology (through the Child Behavior Checklist). Similarity of interregional profiles of group differences in surface area and prenatal cell-specific gene expression was assessed.RESULTS: Across the 11 cortical regions, group differences in cortical area for attention-deficit/hyperactivity disorder, schizophrenia, and Child Behavior Checklist were dominant in multimodal association cortices. The same interregional profiles were also associated with interregional profiles of (prenatal) gene expression specific to proliferative cells, namely radial glia and intermediate progenitor cells (greater expression, larger difference), as well as differentiated cells, namely excitatory neurons and endothelial and mural cells (greater expression, smaller difference). Finally, these cell types were implicated in known pre/perinatal risk factors for psychosis. Genes coexpressed with radial glia were enriched with genes implicated in congenital abnormalities, birth weight, hypoxia, and starvation. Genes coexpressed with endothelial and mural genes were enriched with genes associated with maternal hypertension and preterm birth.CONCLUSIONS: Our findings support a neurodevelopmental model of vulnerability to mental illness whereby prenatal risk factors acting through cell-specific processes lead to deviations from typical brain development during pregnancy.",

keywords = "Attention Deficit Disorder with Hyperactivity, Autism Spectrum Disorder/genetics, Bipolar Disorder, Cerebral Cortex, Child, Depressive Disorder, Major/pathology, Female, Humans, Infant, Newborn, Magnetic Resonance Imaging/methods, Pregnancy, Premature Birth/pathology",

author = "Yash Patel and Jean Shin and Christoph Ab{\'e} and Ingrid Agartz and Clara Alloza and Dag Aln{\ae}s and Sonia Ambrogi and Antonucci, {Linda A} and Celso Arango and Volker Arolt and Guillaume Auzias and Rosa Ayesa-Arriola and Nerisa Banaj and Tobias Banaschewski and Cibele Bandeira and Zeynep Ba{\c s}g{\"o}ze and Cupertino, {Renata Basso} and Bau, {Claiton H D} and Jochen Bauer and Sarah Baumeister and Fabio Bernardoni and Alessandro Bertolino and Bonnin, {Caterina Del Mar} and Daniel Brandeis and Silvia Brem and Jason Bruggemann and Robin B{\"u}low and Bustillo, {Juan R} and Sara Calderoni and Rosa Calvo and Canales-Rodr{\'i}guez, {Erick J} and Cannon, {Dara M} and Susanna Carmona and Carr, {Vaughan J} and Catts, {Stanley V} and Sneha Chenji and Chew, {Qian Hui} and David Coghill and Connolly, {Colm G} and Annette Conzelmann and Craven, {Alexander R} and Benedicto Crespo-Facorro and Kathryn Cullen and Andreas Dahl and Udo Dannlowski and Davey, {Christopher G} and Christine Deruelle and D{\'i}az-Caneja, {Covadonga M} and Katharina Dohm and David Willinger",

note = "Publisher Copyright: {\textcopyright} 2022 Society of Biological Psychiatry",

year = "2022",

month = aug,

day = "15",

doi = "10.1016/j.biopsych.2022.02.959",

language = "English",

volume = "92",

pages = "299--313",

journal = "Biological Psychiatry",

issn = "0006-3223",

publisher = "Elsevier Inc.",

number = "4",

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Patel, Y, Shin, J, Abé, C, Agartz, I, Alloza, C, Alnæs, D, Ambrogi, S, Antonucci, LA, Arango, C, Arolt, V, Auzias, G, Ayesa-Arriola, R, Banaj, N, Banaschewski, T, Bandeira, C, Başgöze, Z, Cupertino, RB, Bau, CHD, Bauer, J, Baumeister, S, Bernardoni, F, Bertolino, A, Bonnin, CDM, Brandeis, D, Brem, S, Bruggemann, J, Bülow, R, Bustillo, JR, Calderoni, S, Calvo, R, Canales-Rodríguez, EJ, Cannon, DM, Carmona, S, Carr, VJ, Catts, SV, Chenji, S, Chew, QH, Coghill, D, Connolly, CG, Conzelmann, A, Craven, AR, Crespo-Facorro, B, Cullen, K, Dahl, A, Dannlowski, U, Davey, CG, Deruelle, C, Díaz-Caneja, CM, Dohm, K & Willinger, D 2022, 'Virtual Ontogeny of Cortical Growth Preceding Mental Illness', Biological Psychiatry, vol. 92, no. 4, pp. 299-313. https://doi.org/10.1016/j.biopsych.2022.02.959

TY - JOUR

T1 - Virtual Ontogeny of Cortical Growth Preceding Mental Illness

AU - Patel, Yash

AU - Shin, Jean

AU - Abé, Christoph

AU - Agartz, Ingrid

AU - Alloza, Clara

AU - Alnæs, Dag

AU - Ambrogi, Sonia

AU - Antonucci, Linda A

AU - Arango, Celso

AU - Arolt, Volker

AU - Auzias, Guillaume

AU - Ayesa-Arriola, Rosa

AU - Banaj, Nerisa

AU - Banaschewski, Tobias

AU - Bandeira, Cibele

AU - Başgöze, Zeynep

AU - Cupertino, Renata Basso

AU - Bau, Claiton H D

AU - Bauer, Jochen

AU - Baumeister, Sarah

AU - Bernardoni, Fabio

AU - Bertolino, Alessandro

AU - Bonnin, Caterina Del Mar

AU - Brandeis, Daniel

AU - Brem, Silvia

AU - Bruggemann, Jason

AU - Bülow, Robin

AU - Bustillo, Juan R

AU - Calderoni, Sara

AU - Calvo, Rosa

AU - Canales-Rodríguez, Erick J

AU - Cannon, Dara M

AU - Carmona, Susanna

AU - Carr, Vaughan J

AU - Catts, Stanley V

AU - Chenji, Sneha

AU - Chew, Qian Hui

AU - Coghill, David

AU - Connolly, Colm G

AU - Conzelmann, Annette

AU - Craven, Alexander R

AU - Crespo-Facorro, Benedicto

AU - Cullen, Kathryn

AU - Dahl, Andreas

AU - Dannlowski, Udo

AU - Davey, Christopher G

AU - Deruelle, Christine

AU - Díaz-Caneja, Covadonga M

AU - Dohm, Katharina

AU - Willinger, David

PY - 2022/8/15

Y1 - 2022/8/15

N2 - BACKGROUND: Morphology of the human cerebral cortex differs across psychiatric disorders, with neurobiology and developmental origins mostly undetermined. Deviations in the tangential growth of the cerebral cortex during pre/perinatal periods may be reflected in individual variations in cortical surface area later in life.METHODS: Interregional profiles of group differences in surface area between cases and controls were generated using T1-weighted magnetic resonance imaging from 27,359 individuals including those with attention-deficit/hyperactivity disorder, autism spectrum disorder, bipolar disorder, major depressive disorder, schizophrenia, and high general psychopathology (through the Child Behavior Checklist). Similarity of interregional profiles of group differences in surface area and prenatal cell-specific gene expression was assessed.RESULTS: Across the 11 cortical regions, group differences in cortical area for attention-deficit/hyperactivity disorder, schizophrenia, and Child Behavior Checklist were dominant in multimodal association cortices. The same interregional profiles were also associated with interregional profiles of (prenatal) gene expression specific to proliferative cells, namely radial glia and intermediate progenitor cells (greater expression, larger difference), as well as differentiated cells, namely excitatory neurons and endothelial and mural cells (greater expression, smaller difference). Finally, these cell types were implicated in known pre/perinatal risk factors for psychosis. Genes coexpressed with radial glia were enriched with genes implicated in congenital abnormalities, birth weight, hypoxia, and starvation. Genes coexpressed with endothelial and mural genes were enriched with genes associated with maternal hypertension and preterm birth.CONCLUSIONS: Our findings support a neurodevelopmental model of vulnerability to mental illness whereby prenatal risk factors acting through cell-specific processes lead to deviations from typical brain development during pregnancy.

AB - BACKGROUND: Morphology of the human cerebral cortex differs across psychiatric disorders, with neurobiology and developmental origins mostly undetermined. Deviations in the tangential growth of the cerebral cortex during pre/perinatal periods may be reflected in individual variations in cortical surface area later in life.METHODS: Interregional profiles of group differences in surface area between cases and controls were generated using T1-weighted magnetic resonance imaging from 27,359 individuals including those with attention-deficit/hyperactivity disorder, autism spectrum disorder, bipolar disorder, major depressive disorder, schizophrenia, and high general psychopathology (through the Child Behavior Checklist). Similarity of interregional profiles of group differences in surface area and prenatal cell-specific gene expression was assessed.RESULTS: Across the 11 cortical regions, group differences in cortical area for attention-deficit/hyperactivity disorder, schizophrenia, and Child Behavior Checklist were dominant in multimodal association cortices. The same interregional profiles were also associated with interregional profiles of (prenatal) gene expression specific to proliferative cells, namely radial glia and intermediate progenitor cells (greater expression, larger difference), as well as differentiated cells, namely excitatory neurons and endothelial and mural cells (greater expression, smaller difference). Finally, these cell types were implicated in known pre/perinatal risk factors for psychosis. Genes coexpressed with radial glia were enriched with genes implicated in congenital abnormalities, birth weight, hypoxia, and starvation. Genes coexpressed with endothelial and mural genes were enriched with genes associated with maternal hypertension and preterm birth.CONCLUSIONS: Our findings support a neurodevelopmental model of vulnerability to mental illness whereby prenatal risk factors acting through cell-specific processes lead to deviations from typical brain development during pregnancy.

KW - Attention Deficit Disorder with Hyperactivity

KW - Autism Spectrum Disorder/genetics

KW - Bipolar Disorder

KW - Cerebral Cortex

KW - Child

KW - Depressive Disorder, Major/pathology

KW - Female

KW - Humans

KW - Infant, Newborn

KW - Magnetic Resonance Imaging/methods

KW - Pregnancy

KW - Premature Birth/pathology

UR - http://www.scopus.com/inward/record.url?scp=85129809360&partnerID=8YFLogxK

U2 - 10.1016/j.biopsych.2022.02.959

DO - 10.1016/j.biopsych.2022.02.959

M3 - Journal article

C2 - 35489875

SN - 0006-3223

VL - 92

SP - 299

EP - 313

JO - Biological Psychiatry

JF - Biological Psychiatry

IS - 4

ER -

Virtual Ontogeny of Cortical Growth Preceding Mental Illness

Abstract

Keywords

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