Dynamic spatiotemporal patterns of brain connectivity reorganize across development

Abstract

Late human development is characterized by the maturation of high-level functional processes, which rely on reshaping of white matter connections, as well as synaptic density. However, the relationship between the whole-brain dynamics and the underlying white matter networks in neurodevelopment is largely unknown. In this study, we focused on how the structural connectome shapes the emerging dynamics of cerebral development between the ages of 6 and 33 years, using functional and diffusion magnetic resonance imaging combined into a spatiotemporal connectivity framework. We defined two new measures of brain dynamics, namely the system diversity and the spatiotemporal diversity, which quantify the level of integration/segregation between functional systems and the level of temporal self-similarity of the functional patterns of brain dynamics, respectively. We observed a global increase in system diversity and a global decrease and local refinement in spatiotemporal diversity values with age. In support of these findings, we further found an increase in the usage of long-range and inter-system white matter connectivity and a decrease in the usage of short-range connectivity with age. These findings suggest that dynamic functional patterns in the brain progressively become more integrative and temporally self-similar with age. These functional changes are supported by a greater involvement of long-range and inter-system axonal pathways.

Large-scale resculpting of cortical circuits in children after surgical resection

“…At the same time, to investigate functional connectivity, we used these localizer fMRI data, rather than resting-state data, to ensure that we were able to elicit sufficiently robust BOLD signal from the young patients. We included a closely age-matched control group, as FC becomes more integrated across development, with the brain shifting from more localized to more global patterns 23 , 24 . We analyzed only the preserved hemisphere in patients, given that heterotopic, intrahemispheric connectivity changes are more likely to be plastic compared with stable homotopic connections which have direct anatomical projections 25 .…”

Ghost Attractors in Spontaneous Brain Activity: Recurrent Excursions Into Functionally-Relevant BOLD Phase-Locking States

“…Assuming this hypothetical scenario, it describes a state-based propagation of the data, rendering the underlying dynamics in a discrete sense (Baker et al, 2014;Karahanoglu and Van De Ville, 2015;Preti et al, 2016;Cabral et al, 2017a). However, other methods have considered dynamic functional connectivity from a continuous point-of-view, such as the spatio-temporal connectome where brain activity is described as a temporal graph (Griffa et al, 2017;Vohryzek et al, 2019) and auto-regressive models (Liégeois et al, 2017). We acknowledge that looking at the brain activity in a discrete sense is only one of the interpretations currently proposed in trying to describe the emergent complex phenomena observed in wholebrain dynamics.…”

Distinct profiles of spatio-temporal brain dynamics along symptoms dimensions in autism

“…For the two groups ASD and CTRL, a series of weakly connected components (CCs) was thus generated. From these series of CCs, SD and STD were estimated (Vohryzek et al 2019) (https://github.com/ivohryzek/STconnectomics_dvlp) at the global scale and at the functional system scale. A summary of the pipeline is presented in (Figure 2).…”

“…Based on the principal of functional co-activation patterns (Tagliazucchi et al 2012; Liu et al 2018), spatio-temporal connectomics approach aims to capture the propagation of functional connectivity on the structural connectome by encoding transient network of spatio-temporal activity (Griffa et al 2017). Two novel dynamics measures, namely system diversity (SD) and spatio-temporal diversity (STD), have been developed to help characterizing this spatio-temporal activity in terms of its diversity of recruitment of cognitive systems (SD) and its spatial self-similarity over time (STD) (Vohryzek et al 2019). SD and STD were shown to capture an increased integration of various functional systems with age along with a higher self-similarity between activity patterns over time suggesting a maturation of the repertoire of integrated spatio-temporal pattern with age (Vohryzek et al 2019), and positively influenced by experience such as schooling (Denervaud et al, Under review).…”

“…Two novel dynamics measures, namely system diversity (SD) and spatio-temporal diversity (STD), have been developed to help characterizing this spatio-temporal activity in terms of its diversity of recruitment of cognitive systems (SD) and its spatial self-similarity over time (STD) (Vohryzek et al 2019). SD and STD were shown to capture an increased integration of various functional systems with age along with a higher self-similarity between activity patterns over time suggesting a maturation of the repertoire of integrated spatio-temporal pattern with age (Vohryzek et al 2019), and positively influenced by experience such as schooling (Denervaud et al, Under review). Despite the evidence of altered brain fluctuations at rest in individuals with ASD, fundamental brain mechanisms reflected by the reorganization of the spatio-temporal activity patterns remain poorly understood, as well as their impact on clinical outcomes.…”