Global topology of human connectome is insensitive to early life environments – A prospective longitudinal study of the general population

Abstract

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