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The interaction between early life complications and a polygenic risk score for schizophrenia is associated with brain activity during emotion processing in healthy participants

Published online by Cambridge University Press:  02 February 2024

Veronica Debora Toro ,
Linda A. Antonucci ,
Tiziana Quarto ,
Roberta Passiatore ,
Leonardo Fazio ,
Gianluca Ursini ,
Qiang Chen ,
Rita Masellis ,
Silvia Torretta  and
Leonardo Sportelli
...Show all authors
Veronica Debora Toro
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy Department of Humanities, University of Foggia, Foggia, Italy
Linda A. Antonucci
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy
Tiziana Quarto
Affiliation:
Department of Humanities, University of Foggia, Foggia, Italy
Roberta Passiatore
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy
Leonardo Fazio
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy Department of Medicine and Surgery, Libera Università Mediterranea “Giuseppe Degennaro”, Bari, Italy
Gianluca Ursini
Affiliation:
Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, USA Department of Psychiatry and Behavioral Sciences, Johns Hopkins University, Baltimore, MD, USA
Qiang Chen
Affiliation:
Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, USA
Rita Masellis
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy U.O.C. Psichiatria Universitaria, Azìenda Ospedaliero-Universitaria Consorziale Policlinico, Bari, Italy
Silvia Torretta
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy
Leonardo Sportelli
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy
Gianluca Christos Kikidis
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy
Francesco Massari
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy
Enrico D'Ambrosio
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy Department of Psychosis Studies, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, SE5 8AF, UK
Antonio Rampino
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy U.O.C. Psichiatria Universitaria, Azìenda Ospedaliero-Universitaria Consorziale Policlinico, Bari, Italy
Giulio Pergola
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, USA
Daniel R. Weinberger
Affiliation:
Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, USA
Alessandro Bertolino
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy U.O.C. Psichiatria Universitaria, Azìenda Ospedaliero-Universitaria Consorziale Policlinico, Bari, Italy
Giuseppe Blasi*
Affiliation:
Psychiatric Neuroscience Group, Department of Translational Biomedicine and Neuroscience, University of Bari “Aldo Moro”, Bari, Italy U.O.C. Psichiatria Universitaria, Azìenda Ospedaliero-Universitaria Consorziale Policlinico, Bari, Italy
*
Corresponding author: Giuseppe Blasi; Email: giuseppe.blasi@uniba.it
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Abstract

Background

Previous evidence suggests that early life complications (ELCs) interact with polygenic risk for schizophrenia (SCZ) in increasing risk for the disease. However, no studies have investigated this interaction on neurobiological phenotypes. Among those, anomalous emotion-related brain activity has been reported in SCZ, even if evidence of its link with SCZ-related genetic risk is not solid. Indeed, it is possible this relationship is influenced by non-genetic risk factors. Thus, this study investigated the interaction between SCZ-related polygenic risk and ELCs on emotion-related brain activity.

Methods

169 healthy participants (HP) in a discovery and 113 HP in a replication sample underwent functional magnetic resonance imaging (fMRI) during emotion processing, were categorized for history of ELCs and genome-wide genotyped. Polygenic risk scores (PRSs) were computed using SCZ-associated variants considering the most recent genome-wide association study. Furthermore, 75 patients with SCZ also underwent fMRI during emotion processing to verify consistency of their brain activity patterns with those associated with risk factors for SCZ in HP.

Results

Results in the discovery and replication samples indicated no effect of PRSs, but an interaction between PRS and ELCs in left ventrolateral prefrontal cortex (VLPFC), where the greater the activity, the greater PRS only in presence of ELCs. Moreover, SCZ had greater VLPFC response than HP.

Conclusions

These results suggest that emotion-related VLPFC response lies in the path from genetic and non-genetic risk factors to the clinical presentation of SCZ, and may implicate an updated concept of intermediate phenotype considering early non-genetic factors of risk for SCZ.

Keywords

early life complicationsemotion processingfacesfMRIpolygenic risk scoreschizophrenia
Type
Original Article
Information
Psychological Medicine , First View , pp. 1 - 10
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Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press

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