Signal diffusion along connectome gradients and inter-hub routing differentially contribute to dynamic human brain function

Park, Bo‐yong; Wael, Reinder Vos de; Paquola, Casey; Larivière, Sara; Benkarim, Oualid; Royer, Jessica; Tavakol, Shahin; Cruces, Raúl R.; Li, Shuyu; Valk, Sofie L.; Margulies, Daniel S.; Mišić, Bratislav; Bzdok, Danilo; Smallwood, Jonathan; Bernhardt, Boris C.

doi:10.1016/j.neuroimage.2020.117429

Cited by 76 publications

(58 citation statements)

References 107 publications

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“…Overall, our results support that lowdimensional eigenmode representations of structural connectivity may potentially underpin intrinsic functional architecture of the human connectome. Such a conclusion is in line with several prior studies in healthy individuals showing that whole-brain structural connectivity gradients shape dynamic signaling at rest (Park et al, 2021) as well as dynamic brain reconfigurations during tasks (C. Murphy et al, 2019).…”

Section: Discussionsupporting

confidence: 91%

Microstructural underpinnings and macroscale functional implications of temporal lobe connectivity gradients

Wael

Royer

Tavakol

et al. 2020

Preprint

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The temporal lobe is implicated in higher cognitive processes and is one of the regions that underwent substantial reorganization during primate evolution. Its functions are instantiated, in part, by its complex layout of structural connections. This study identified low-dimensional representations of structural connectivity variations in human temporal cortex and explored their microstructural underpinnings and associations to macroscale function. We identified three eigenmodes which described gradients in structural connectivity. These gradients reflected interregional variations in cortical microstructure derived from quantitative MRI and post-mortem histology. Gradient-informed models accurately predicted macroscale measures of temporal lobe function. Gradients aligned closely with established measures of functional reconfiguration and areal expansion between macaques and humans, highlighting the important role evolution has played in shaping temporal lobe function. Our results provide robust evidence for three axes of structural connectivity in human temporal cortex with consistent microstructural underpinnings and contributions to large-scale brain network function.

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Section: Discussionsupporting

confidence: 91%

Microstructural underpinnings and macroscale functional implications of temporal lobe connectivity gradients

Wael

Royer

Tavakol

et al. 2020

Preprint

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“…The structural connectome was built by mapping the reconstructed cross-section streamlines onto the Schaefer 7-network based atlas with 200 parcels (Schaefer et al, 2018) then log-transformed to adjust for the scale (Fornito et al, 2016). We opted for this atlas as it (i) allows contextualization of our findings within macroscale intrinsic functional communities (Yeo et al, 2011), (ii) incorporates the option to assess results across different granularities, and (iii) aligns the current study with previous work from our group (Benkarim et al, 2020;Paquola et al, 2020;Park et al, 2021Park et al, , 2020aRodríguez-Cruces et al, 2020) and others (Baum et al, 2020;Betzel et al, 2019;Osmanlıoğlu et al, 2019).…”

Section: Structural Connectome Manifold Identificationmentioning

confidence: 99%

“…In addition, these techniques capture multiple, potentially overlapping gradients in connectivity along cortical mantle, which can represent both subregional heterogeneity and multiplicity within a brain region (Haak and Beckmann, 2020). In prior work, we showed that multiple dMRI gradients can illustrate structural underpinnings of dynamic functional communication in the adult human connectome (Park et al, 2021). In line with prior conceptual accounts, the low-dimensional eigenvectors (i.e., gradients) derived from these techniques provide continuous dimensions of cortical organization, and thus the eigenvectors can jointly generate intrinsic coordinate systems of the brain based on connectivity (Bijsterbosch et al, 2020;Haak et al, 2018;Huntenburg et al, 2018;Margulies et al, 2016;Mars et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

“…Beyond these methodological considerations, prior work has shown that the principal gradients estimated from resting-state functional (Margulies et al, 2016), microstructural (Paquola et al, 2019b), and diffusion MRI (Park et al, 2020a) all converge broadly along an established model of sensory-fugal hierarchy and laminar differentiation (Mesulam, 1998), allowing gradient mapping techniques to make conceptual contact to theories of cortical organization, development, and evolution (Buckner and Krienen, 2013;Goulas et al, 2018;Huntenburg et al, 2018;Sanides, 1969Sanides, , 1962). An emerging literature has indeed shown utility of the gradient framework to study primate evolution and cross-species alignment (Blazquez Freches et al, 2020;, neurodevelopment (Hong et al, 2019;Paquola et al, 2019a), as well as plasticity and structure-function coupling (Park et al, 2021;Vázquez-Rodríguez et al, 2019). In a recent assessment by our team, manifold learning techniques have been applied to myelin sensitive intracortical MT data, showing an increasing myeloarchitectural differentiation of association cortex throughout adolescence (Paquola et al, 2019a).…”

Section: Introductionmentioning

confidence: 99%

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An expanding manifold in transmodal regions characterizes adolescent reconfiguration of structural connectome organization

Park¹,

Bethlehem²,

Paquola³

et al. 2021

eLife

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Adolescence is a critical time for the continued maturation of brain networks. Here, we assessed structural connectome development in a large longitudinal sample ranging from childhood to young adulthood. By projecting high-dimensional connectomes into compact manifold spaces, we identified a marked expansion of structural connectomes with the strongest effects in transmodal regions during adolescence. Findings reflected increased within-module connectivity together with increased segregation, indicating increasing differentiation of higher-order association networks from the rest of the brain. Projection of subcortico-cortical connectivity patterns into these manifolds showed parallel alterations in pathways centered on the caudate and thalamus. Connectome findings were contextualized via spatial transcriptome association analysis, highlighting genes enriched in cortex, thalamus, and striatum. Statistical learning of cortical and subcortical manifold features at baseline and their maturational change predicted measures of intelligence at follow-up. Our findings demonstrate that connectome manifold learning can bridge the conceptual and empirical gaps between macroscale network reconfigurations, microscale processes, and cognitive outcomes in adolescent development.

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“…Furthermore, functional connectome findings suggest their promise to serve as spatial axes aligned with the cortical hierarchy (Margulies et al, 2016; Mesulam, 1998) and to capture functional activation patterns across different task states (Karapanagiotidis et al, 2020; Mckeown et al, 2020). A recent study furthermore demonstrated that the application of manifold learning techniques to whole-brain dMRI connectomes is feasible, and that these gradients provide a coordinate system to interrogate the coupling between brain structure and functional dynamics (Park et al, 2021). Still, the application of manifold techniques to dMRI connectomes in children and adolescents to track their longitudinal maturations has not been performed.…”

Section: Introductionmentioning

confidence: 99%

An expanding manifold in transmodal regions characterizes adolescent reconfiguration of structural connectome organization

Park

Bethlehem

Paquola

et al. 2020

Preprint

Self Cite

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Adolescence is a critical time for the continued maturation of brain networks, and the current work assessed longitudinal reconfigurations of diffusion MRI derived connectomes in a large sample (n = 208). We identified an expansion of structural network representations in lower dimensional manifold spaces, with strongest effects in transmodal cortices and indicative of an increasing differentiation of these networks from the rest of the brain. Findings were shown to relate to mainly an increase in within-module connectivity and increased segregation during adolescence. Connectome findings were consistent when additionally controlling for regional changes in MRI measures of cortical morphology and myelin, despite reductions in effect sizes. On the other hand, cortical areas showing manifold expansion were found to become more closely embedded with subcortical targets, notably the striatum. Identified networks were also found to harbor genes significantly expressed in both cortical and subcortical regions. Using supervised machine learning with cross-validation, we demonstrated that cortico-subcortical manifold features at baseline and their maturational change predicted measures of intelligence at follow-up. Our findings chart adolescent connectome development and suggest that brain-wide network reconfigurations offer intermediary phenotypes between genetic-microstructural processes and cognitive-behavioral outcomes.We explored how whole-brain structural networks reconfigure during adolescence, using a novel analysis that simultaneously interrogates network and regional features. Our approach revealed an increasing differentiation of the connectome during this critical period, particularly in higher-order prefrontal and parietal regions. We could show that while this effect was only partially related to developmental trajectories of intracortical microstructure and morphology, but rather to changes in connectivity to subcortical areas, particularly the striatum. Cortico-subcortical network effects were also supported by transcriptomics and phenotype prediction, which suggested that cognitive function in adulthood was most effectively predicted when combining cortical and subcortical features. Our findings shed new light on adolescence and support a key role of cortico-subcortical integration in shaping macroscale structural networks. Park et al. | Structural connectome maturation during adolescence 3 3

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Signal diffusion along connectome gradients and inter-hub routing differentially contribute to dynamic human brain function

Cited by 76 publications

References 107 publications

Microstructural underpinnings and macroscale functional implications of temporal lobe connectivity gradients

Microstructural underpinnings and macroscale functional implications of temporal lobe connectivity gradients

An expanding manifold in transmodal regions characterizes adolescent reconfiguration of structural connectome organization

An expanding manifold in transmodal regions characterizes adolescent reconfiguration of structural connectome organization

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