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Early adversity changes the economic conditions of structural brain network organisation

View ORCID ProfileSofia Carozza, View ORCID ProfileJoni Holmes, View ORCID ProfilePetra E. Vértes, View ORCID ProfileEd Bullmore, View ORCID ProfileTanzil M. Arefin, Alexa Pugliese, Jiangyang Zhang, View ORCID ProfileArie Kaffman, View ORCID ProfileDanyal Akarca, View ORCID ProfileDuncan E. Astle
doi: https://doi.org/10.1101/2022.06.08.495303
Sofia Carozza
1MRC Cognition and Brain Sciences Unit, University of Cambridge, Cambridge, UK
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  • For correspondence: sofia.carozza@mrc-cbu.cam.ac.uk
Joni Holmes
1MRC Cognition and Brain Sciences Unit, University of Cambridge, Cambridge, UK
2School of Psychology, University of East Anglia, Norwich, UK
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Petra E. Vértes
3Department of Psychiatry, University of Cambridge, Cambridge, UK
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Ed Bullmore
3Department of Psychiatry, University of Cambridge, Cambridge, UK
4Department of Clinical Neurosciences, Wolfson Brain Imaging Centre, University of Cambridge, Cambridge, UK
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Tanzil M. Arefin
5Bernard and Irene Schwartz Center for Biomedical Imaging, Department of Radiology, New York University School of Medicine, New York, NY 10016, USA
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Alexa Pugliese
6Department of Psychiatry, Yale University School of Medicine, 300 George Street, Suite 901, New Haven CT, 06511, USA
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Jiangyang Zhang
5Bernard and Irene Schwartz Center for Biomedical Imaging, Department of Radiology, New York University School of Medicine, New York, NY 10016, USA
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Arie Kaffman
6Department of Psychiatry, Yale University School of Medicine, 300 George Street, Suite 901, New Haven CT, 06511, USA
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Danyal Akarca
1MRC Cognition and Brain Sciences Unit, University of Cambridge, Cambridge, UK
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Duncan E. Astle
1MRC Cognition and Brain Sciences Unit, University of Cambridge, Cambridge, UK
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Abstract

Early adversity can change educational, cognitive, and mental health outcomes. However, the neural processes through which early adversity exerts these effects remain largely unknown. We used generative network modelling of the mouse connectome to test whether unpredictable postnatal stress shifts the constraints that govern the formation of the structural connectome. A model that trades off the wiring cost of long-distance connections with topological homophily (i.e. links between regions with shared neighbours) generated simulations that replicate the organisation of the rodent connectome. The imposition of early life adversity significantly shifted the best-performing parameter combinations toward zero, heightening the stochastic nature of the generative process. Put simply, unpredictable postnatal stress changes the economic constraints that shape network formation, introducing greater randomness into the structural development of the brain. While this change may constrain the development of cognitive abilities, it could also reflect an adaptive mechanism. In other words, neural development could harness heightened stochasticity to make networks more robust to perturbation, thereby facilitating effective responses to future threats and challenges.

Significance statement Children who experience adversity early in life – such as chronic poverty or abuse – show numerous neural differences that are linked to poorer cognition and mental health later in life. To effectively mitigate the burden of adversity, it is critical to identify how these differences arise. In this paper, we use computational modelling to test whether growing up in an impoverished and unpredictable environment changes the development of structural connections in the mouse brain. We found that early adversity appears to introduce more stochasticity in the formation of neural architecture. Our findings point to a potential mechanism for how early adversity could change the course of child development.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Several references to Figure 5 were updated with the correct numbering and lettering.

  • https://osf.io/evgw5/

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted June 11, 2022.
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Early adversity changes the economic conditions of structural brain network organisation
Sofia Carozza, Joni Holmes, Petra E. Vértes, Ed Bullmore, Tanzil M. Arefin, Alexa Pugliese, Jiangyang Zhang, Arie Kaffman, Danyal Akarca, Duncan E. Astle
bioRxiv 2022.06.08.495303; doi: https://doi.org/10.1101/2022.06.08.495303
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Early adversity changes the economic conditions of structural brain network organisation
Sofia Carozza, Joni Holmes, Petra E. Vértes, Ed Bullmore, Tanzil M. Arefin, Alexa Pugliese, Jiangyang Zhang, Arie Kaffman, Danyal Akarca, Duncan E. Astle
bioRxiv 2022.06.08.495303; doi: https://doi.org/10.1101/2022.06.08.495303

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