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Research Articles, Development/Plasticity/Repair

Longitudinal Allometry of Sulcal Morphology in Health and Schizophrenia

Joost Janssen, Clara Alloza, Covadonga M. Díaz-Caneja, Javier Santonja, Laura Pina-Camacho, Pedro M. Gordaliza, Alberto Fernández-Pena, Noemi González Lois, Elizabeth E.L. Buimer, Neeltje E.M. van Haren, Wiepke Cahn, Eduard Vieta, Josefina Castro-Fornieles, Miquel Bernardo, Celso Arango, René S. Kahn, Hilleke E. Hulshoff Pol and Hugo G. Schnack
Journal of Neuroscience 4 May 2022, 42 (18) 3704-3715; DOI: https://doi.org/10.1523/JNEUROSCI.0606-21.2022
Joost Janssen
1Department of Child and Adolescent Psychiatry, Institute of Psychiatry and Mental Health, Hospital General Universitario Gregorio Marañón, 28007 Madrid, Spain
2Instituto de Investigación Sanitaria Gregorio Marañón, 28007 Madrid, Spain
3Ciber del Área de Salud Mental, 28007 Madrid, Spain
4Department of Psychiatry, UMCU Brain Center, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands
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  • ORCID record for Joost Janssen
Clara Alloza
1Department of Child and Adolescent Psychiatry, Institute of Psychiatry and Mental Health, Hospital General Universitario Gregorio Marañón, 28007 Madrid, Spain
2Instituto de Investigación Sanitaria Gregorio Marañón, 28007 Madrid, Spain
3Ciber del Área de Salud Mental, 28007 Madrid, Spain
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Covadonga M. Díaz-Caneja
1Department of Child and Adolescent Psychiatry, Institute of Psychiatry and Mental Health, Hospital General Universitario Gregorio Marañón, 28007 Madrid, Spain
2Instituto de Investigación Sanitaria Gregorio Marañón, 28007 Madrid, Spain
3Ciber del Área de Salud Mental, 28007 Madrid, Spain
5School of Medicine, Universidad Complutense, 28040 Madrid, Spain
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Javier Santonja
1Department of Child and Adolescent Psychiatry, Institute of Psychiatry and Mental Health, Hospital General Universitario Gregorio Marañón, 28007 Madrid, Spain
2Instituto de Investigación Sanitaria Gregorio Marañón, 28007 Madrid, Spain
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Laura Pina-Camacho
1Department of Child and Adolescent Psychiatry, Institute of Psychiatry and Mental Health, Hospital General Universitario Gregorio Marañón, 28007 Madrid, Spain
2Instituto de Investigación Sanitaria Gregorio Marañón, 28007 Madrid, Spain
3Ciber del Área de Salud Mental, 28007 Madrid, Spain
5School of Medicine, Universidad Complutense, 28040 Madrid, Spain
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Pedro M. Gordaliza
6Departamento de Bioingeniería e Ingeniería Aeroespacial, Universidad Carlos III de Madrid, 28911 Madrid, Spain
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Alberto Fernández-Pena
2Instituto de Investigación Sanitaria Gregorio Marañón, 28007 Madrid, Spain
6Departamento de Bioingeniería e Ingeniería Aeroespacial, Universidad Carlos III de Madrid, 28911 Madrid, Spain
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Noemi González Lois
1Department of Child and Adolescent Psychiatry, Institute of Psychiatry and Mental Health, Hospital General Universitario Gregorio Marañón, 28007 Madrid, Spain
2Instituto de Investigación Sanitaria Gregorio Marañón, 28007 Madrid, Spain
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Elizabeth E.L. Buimer
4Department of Psychiatry, UMCU Brain Center, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands
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Neeltje E.M. van Haren
4Department of Psychiatry, UMCU Brain Center, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands
7Department of Child and Adolescent Psychiatry/Psychology, Erasmus University Medical Centre, Sophia Children's Hospital, 3015 GD Rotterdam, The Netherlands
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Wiepke Cahn
4Department of Psychiatry, UMCU Brain Center, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands
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Eduard Vieta
3Ciber del Área de Salud Mental, 28007 Madrid, Spain
9Bipolar Disorders Unit, Clinical Institute of Neurosciences, Hospital Clínic, University of Barcelona, Institut d'Investigacions Biomèdiques August Pi i Sunyer, 08036 Barcelona, Spain
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Josefina Castro-Fornieles
3Ciber del Área de Salud Mental, 28007 Madrid, Spain
10Department of Child and Adolescent Psychiatry and Psychology, Clinical Institute of Neurosciences, Hospital Clínic, University of Barcelona, Institut d'Investigacions Biomèdiques August Pi i Sunyer, 08036 Barcelona, Spain
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Miquel Bernardo
3Ciber del Área de Salud Mental, 28007 Madrid, Spain
8Barcelona Clinic Schizophrenia Unit, Hospital Clinic of Barcelona, Neuroscience Institute, Institut d'Investigacions Biomèdiques August Pi i Sunyer, University of Barcelona, 08036 Barcelona, Spain
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Celso Arango
1Department of Child and Adolescent Psychiatry, Institute of Psychiatry and Mental Health, Hospital General Universitario Gregorio Marañón, 28007 Madrid, Spain
2Instituto de Investigación Sanitaria Gregorio Marañón, 28007 Madrid, Spain
3Ciber del Área de Salud Mental, 28007 Madrid, Spain
5School of Medicine, Universidad Complutense, 28040 Madrid, Spain
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René S. Kahn
4Department of Psychiatry, UMCU Brain Center, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands
11Department of Psychiatry, Icahn School of Medicine at Mount Sinai, 10029 New York
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Hilleke E. Hulshoff Pol
4Department of Psychiatry, UMCU Brain Center, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands
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Hugo G. Schnack
4Department of Psychiatry, UMCU Brain Center, University Medical Center Utrecht, 3584 CX Utrecht, The Netherlands
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Abstract

Scaling between subcomponents of folding and total brain volume (TBV) in healthy individuals (HIs) is allometric. It is unclear whether this is true in schizophrenia (SZ) or first-episode psychosis (FEP). This study confirmed normative allometric scaling norms in HIs using discovery and replication samples. Cross-sectional and longitudinal diagnostic differences in folding subcomponents were then assessed using an allometric framework. Structural imaging from a longitudinal (Sample 1: HI and SZ, nHI Baseline = 298, nSZ Baseline = 169, nHI Follow-up = 293, nSZ Follow-up = 168, totaling 1087 images, all individuals ≥ 2 images, age 16-69 years) and a cross-sectional sample (Sample 2: nHI = 61 and nFEP = 89, age 10-30 years), all human males and females, is leveraged to calculate global folding and its nested subcomponents: sulcation index (SI, total sulcal/cortical hull area) and determinants of sulcal area: sulcal length and sulcal depth. Scaling of SI, sulcal area, and sulcal length with TBV in SZ and FEP was allometric and did not differ from HIs. Longitudinal age trajectories demonstrated steeper loss of SI and sulcal area through adulthood in SZ. Longitudinal allometric analysis revealed that both annual change in SI and sulcal area was significantly stronger related to change in TBV in SZ compared with HIs. Our results detail the first evidence of the disproportionate contribution of changes in SI and sulcal area to TBV changes in SZ. Longitudinal allometric analysis of sulcal morphology provides deeper insight into lifespan trajectories of cortical folding in SZ.

SIGNIFICANCE STATEMENT Psychotic disorders are associated with deficits in cortical folding and brain size, but we lack knowledge of how these two morphometric features are related. We leverage cross-sectional and longitudinal samples in which we decompose folding into a set of nested subcomponents: sulcal and hull area, and sulcal depth and length. We reveal that, in both schizophrenia and first-episode psychosis, (1) scaling of subcomponents with brain size is different from expected scaling laws and (2) caution is warranted when interpreting results from traditional methods for brain size correction. Longitudinal allometric scaling points to loss of sulcal area as a principal contributor to loss of brain size in schizophrenia. These findings advance the understanding of cortical folding atypicalities in psychotic disorders.

  • allometry
  • cortical folding
  • first-episode psychosis
  • longitudinal
  • schizophrenia
  • sulcus

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The Journal of Neuroscience: 42 (18)
Journal of Neuroscience
Vol. 42, Issue 18
4 May 2022
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Longitudinal Allometry of Sulcal Morphology in Health and Schizophrenia
Joost Janssen, Clara Alloza, Covadonga M. Díaz-Caneja, Javier Santonja, Laura Pina-Camacho, Pedro M. Gordaliza, Alberto Fernández-Pena, Noemi González Lois, Elizabeth E.L. Buimer, Neeltje E.M. van Haren, Wiepke Cahn, Eduard Vieta, Josefina Castro-Fornieles, Miquel Bernardo, Celso Arango, René S. Kahn, Hilleke E. Hulshoff Pol, Hugo G. Schnack
Journal of Neuroscience 4 May 2022, 42 (18) 3704-3715; DOI: 10.1523/JNEUROSCI.0606-21.2022

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Longitudinal Allometry of Sulcal Morphology in Health and Schizophrenia
Joost Janssen, Clara Alloza, Covadonga M. Díaz-Caneja, Javier Santonja, Laura Pina-Camacho, Pedro M. Gordaliza, Alberto Fernández-Pena, Noemi González Lois, Elizabeth E.L. Buimer, Neeltje E.M. van Haren, Wiepke Cahn, Eduard Vieta, Josefina Castro-Fornieles, Miquel Bernardo, Celso Arango, René S. Kahn, Hilleke E. Hulshoff Pol, Hugo G. Schnack
Journal of Neuroscience 4 May 2022, 42 (18) 3704-3715; DOI: 10.1523/JNEUROSCI.0606-21.2022
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Keywords

  • allometry
  • cortical folding
  • first-episode psychosis
  • longitudinal
  • schizophrenia
  • sulcus

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