TY - JOUR
T1 - Global topology of human connectome is insensitive to early life environments – A prospective longitudinal study of the general population
AU - Carozza, Sofia
AU - Holmes, Joni
AU - Akarca, Danyal
AU - Astle, Duncan E.
N1 - Funding information: The UK Medical Research Council and the Wellcome Trust (Grant ref: 217065/Z/19/Z) and the University of Bristol provide core support for ALSPAC. A comprehensive list of grants funding is available on the ALSPAC website (www.bristol.ac.uk/alspac/external/documents/grant-acknowledgements.pdf). Measures used in this study were funded by an MRC and Wellcome grant to George Davey Smith (Grant ref: 076467/Z/05/Z) and a Wellcome grant to Glyn Lewis (Grant ref: 08426812/Z/07/Z). This publication is the work of the authors, whose work was funded by a Cambridge Marshall Scholarship to SC, MRC intramural award G101400 to JH, MRC programme grant MC-A060-5PQ40 to DEA, JSMF Opportunity Award to DEA, and TWCF Grant 0159 to DEA. SC will serve as guarantor for the contents of this paper.
Rights retention statement: For the purpose of open access, the author has applied a Creative Commons Attribution (CC BY) licence to any Author Accepted Manuscript version arising from this submission.
PY - 2024/7
Y1 - 2024/7
N2 - The widely acknowledged detrimental impact of early adversity on child development has driven efforts to understand the underlying mechanisms that may mediate these effects within the developing brain. Recent efforts have begun to move beyond associating adversity with the morphology of individual brain regions towards determining if and how adversity might shape their interconnectivity. However, whether adversity effects a global shift in the organisation of whole-brain networks remains unclear. In this study, we assessed this possibility using parental questionnaire and diffusion imaging data from The Avon Longitudinal Study of Parents and Children (ALSPAC, N = 913), a prospective longitudinal study spanning more than 20 years. We tested whether a wide range of adversities—including experiences of abuse, domestic violence, physical and emotional cruelty, poverty, neglect, and parental separation—measured by questionnaire within the first seven years of life were significantly associated with the tractography-derived connectome in young adulthood. We tested this across multiple measures of organisation and using a computational model that simulated the wiring economy of the brain. We found no significant relationships between early exposure to any form of adversity and the global organisation of the structural connectome in young adulthood. We did detect local differences in the medial prefrontal cortex, as well as an association between weaker brain wiring constraints and greater externalising behaviour in adolescence. Our results indicate that further efforts are necessary to delimit the magnitude and functional implications of adversity-related differences in connectomic organization. Research Highlights: Diverse prospective measures of the early-life environment do not predict the organisation of the DTI tractography-derived connectome in young adulthood Wiring economy of the connectome is weakly associated with externalising in adolescence, but not internalising or cognitive ability Further work is needed to establish the scope and significance of global adversity-related differences in the structural connectome.
AB - The widely acknowledged detrimental impact of early adversity on child development has driven efforts to understand the underlying mechanisms that may mediate these effects within the developing brain. Recent efforts have begun to move beyond associating adversity with the morphology of individual brain regions towards determining if and how adversity might shape their interconnectivity. However, whether adversity effects a global shift in the organisation of whole-brain networks remains unclear. In this study, we assessed this possibility using parental questionnaire and diffusion imaging data from The Avon Longitudinal Study of Parents and Children (ALSPAC, N = 913), a prospective longitudinal study spanning more than 20 years. We tested whether a wide range of adversities—including experiences of abuse, domestic violence, physical and emotional cruelty, poverty, neglect, and parental separation—measured by questionnaire within the first seven years of life were significantly associated with the tractography-derived connectome in young adulthood. We tested this across multiple measures of organisation and using a computational model that simulated the wiring economy of the brain. We found no significant relationships between early exposure to any form of adversity and the global organisation of the structural connectome in young adulthood. We did detect local differences in the medial prefrontal cortex, as well as an association between weaker brain wiring constraints and greater externalising behaviour in adolescence. Our results indicate that further efforts are necessary to delimit the magnitude and functional implications of adversity-related differences in connectomic organization. Research Highlights: Diverse prospective measures of the early-life environment do not predict the organisation of the DTI tractography-derived connectome in young adulthood Wiring economy of the connectome is weakly associated with externalising in adolescence, but not internalising or cognitive ability Further work is needed to establish the scope and significance of global adversity-related differences in the structural connectome.
KW - ALSPAC
KW - connectome
KW - early adversity
KW - generative network modelling
KW - graph theory
KW - structural connectivity
UR - http://www.scopus.com/inward/record.url?scp=85188452450&partnerID=8YFLogxK
U2 - 10.1111/desc.13490
DO - 10.1111/desc.13490
M3 - Article
AN - SCOPUS:85188452450
VL - 27
JO - Developmental Science
JF - Developmental Science
SN - 1363-755X
IS - 4
M1 - e13490
ER -