Functional connectome contractions in temporal lobe epilepsy: microstructural underpinnings and associations to surgical outcome

Larivière, Sara; Wang, Yifei; Wael, Reinder Vos de; Frauscher, Birgit; Wang, Zhengge; Bernasconi, Andrea; Bernasconi, Neda; Schrader, Dewi; Zhang, Zhiqiang; Bernhardt, Boris C.

doi:10.1101/756494

Cited by 8 publications

(5 citation statements)

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“…Irrespective of cortical or subcortical involvement, the vulnerability of hub regions to grey matter atrophy can be partly ascribed to their disproportionate number of connections and diffuse effect on structural and functional networks (Fornito et al, 2015). Thus, a targeted hub attack, as in the case of epilepsyrelated atrophy, may fragment and segregate the network, favoring recurrent seizure activity in temporal lobe and idiopathic generalized epilepsies (Albert et al, 2000;Lariviere et al, 2019b;Larivière et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

Network-based atrophy modelling in the common epilepsies: a worldwide ENIGMA study

Larivière

Rodríguez‐Cruces

Royer

et al. 2020

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Epilepsy is increasingly conceptualized as a network disorder. In this cross-sectional megaanalysis, we integrated neuroimaging and connectome analysis to identify network associations with atrophy patterns in 1,021 adults with epilepsy compared to 1,564 healthy controls from 19 international sites. In temporal lobe epilepsy, areas of atrophy co-localized with highly interconnected cortical hub regions, whereas idiopathic generalized epilepsy showed preferential subcortical hub involvement. These morphological abnormalities were anchored to the connectivity profiles of distinct disease epicenters, pointing to temporo-limbic cortices in temporal lobe epilepsy and fronto-central cortices in idiopathic generalized epilepsy. Indices of progressive atrophy further revealed a strong influence of connectome architecture on disease progression in temporal lobe, but not idiopathic generalized, epilepsy. Our findings were reproduced across individual sites and single patients, and were robust across different analytical methods. Through worldwide collaboration in ENIGMA-Epilepsy, we provided novel insights into the macroscale features that shape the pathophysiology of common epilepsies.Larivière et al.Atrophy modelling in the common epilepsies | 4

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Section: Discussionmentioning

confidence: 99%

Network-based atrophy modelling in the common epilepsies: a worldwide ENIGMA study

Larivière

Rodríguez‐Cruces

Royer

et al. 2020

Preprint

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“…For each node, we matched the exemplar vertex to the nearest voxel in volumetric space, then used a Chamfer propagation (imGeodesics Toolbox; https://github.com/mattools/matImage/wiki/imGeodesics) to calculate the distance to all other voxels travelling through a grey/white matter mask. This approach differs from previous implementations of geodesic distance 28,29,37 by involving paths through the grey and white matter, allowing for jumps within gyri and interhemispheric projections 102 . We projected GD estimations back from volumetric to surface space, averaged within node and produced a 200☓200 GD matrix.…”

Section: Geodesic Distancementioning

confidence: 99%

A cortical wiring space links cellular architecture, functional dynamics and hierarchies in humans

Paquola

Seidlitz

Benkarim

et al. 2020

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The vast net of fibres within and underneath the cortical mantle is optimised to support the convergence of different levels of brain organisation, specifically through linking cellular and architectural features of different cortical areas to give rise to more integrated neural function. Leveraging multimodal neuroimaging and machine learning techniques, we identified a novel manifold space that is governed by geometric, microstructural, and connectional aspects of cortico-cortical wiring. Principal dimensions of this manifold recapitulated established sensory-limbic and anterior-posterior gradients of brain organisation, and were found to reflect neural and glial gradients of cytoarchitectural organisation and gene expression. Manifold features were accurate in predicting cortico-cortical functional interactions derived from resting-state functional neuroimaging. Furthermore, application of this approach to a group of neurological patients, who underwent intracerebral encephalographic recordings, established that manifold features also explained the direction of information flow between different cortical areas. These results advance our understanding of how cell-specific neurobiological gradients produce a hierarchical cortical wiring scheme that is concordant with increasing functional sophistication of human brain organisation. RESULTSA multi-scale model of cortical wiring The wiring model was first derived from a Discovery subset of the Human Connectome Project dataset (n=100 unrelated adults) that offers high resolution structural magnetic resonance imaging (MRI), diffusion MRI, and microstructurally sensitive T1w/T2w maps 38 (Figure 1A, see Methods for details). and diffusion-based tractography strength (TS) were estimated between all pairs of nodes. (B) Normalised matrices were concatenated and transformed into an affinity matrix. Manifold learning identified a lower dimensional representation of cortical wiring. (C) Left. Node positions in this newly-discovered structural manifold, coloured according to proximity to axis limits. Closeness to the maximum of the second eigenvector is redness, towards the minimum of the first eigenvector is greenness and towards the maximum of the first eigenvector is blueness. The first two eigenvectors are shown on the respective axes. Right. Equivalent cortical surface representation. (D) Calculation of inter-regional distances in the structural manifold from specific seeds to other regions of cortex (left). Overall distance to all other nodes can also be quantified to index centrality of different regions, with more integrative areas having shorter distances to nodes (right). Figure 4: Hierarchical information processing is organised by the structural manifold. (A)Intracerebral implantations of ten epileptic patients were mapped to cortical surface. Intracortical EEG recordings were selected across five minutes of rest. (B) Boxplots show the variance explained in coherence by the structural manifold using adaboost machine learning across all nodes. (C) The phase slope ...

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“…n, Leveraging advanced manifold learning, we depicted macroscale connectome organization along continuous cortical axes. Similar approaches have previously been harnessed to decompose microstructural 21,45 , and functional 10,[41][42][43]48,49,[75][76][77] and dMRI connectomes 51 . These techniques are appealing, as they offer a low dimensional perspective on connectome reconfigurations in a datadriven and spatially unconstrained manner.…”

Section: Iqmentioning

confidence: 99%

“…2A). To assess how manifold eccentricity changes related to connectome topology, we calculated degree centrality, as well as modular measures of within-module degree and participation coefficient using the Brain Connectivity Toolbox (https://sites.google.com/site/bctnet/) 70 and connectivity distance using a recently published approach 77 . Degree centrality is defined as the row-wise sum of the weighted connectivity matrix, representing the connection strength of a given node 70 .…”

Section: Association With Connectome Topologymentioning

confidence: 99%

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

Park

Bethlehem

Paquola

et al. 2020

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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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Functional connectome contractions in temporal lobe epilepsy: microstructural underpinnings and associations to surgical outcome

Cited by 8 publications

References 58 publications

Network-based atrophy modelling in the common epilepsies: a worldwide ENIGMA study

Network-based atrophy modelling in the common epilepsies: a worldwide ENIGMA study

A cortical wiring space links cellular architecture, functional dynamics and hierarchies in humans

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

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