Core and matrix thalamic sub-populations relate to spatio-temporal cortical connectivity gradients

Müller, Eli J.; Munn, Brandon; Hearne, Luke J.; Smith, Jared B.; Fulcher, Ben D.; Arnatkevičiūtė, Aurina; Lurie, Daniel J.; Cocchi, Luca; Shine, James M.

doi:10.1016/j.neuroimage.2020.117224

Cited by 82 publications

(103 citation statements)

References 71 publications

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“…More generally, the present findings are part of a larger trend in the field to understand structure-function relationships by considering molecular ( Richiardi et al, 2015 ; Fulcher and Fornito, 2016 ; Anderson et al, 2018 ; Zheng et al, 2019 ), cellular ( Scholtens et al, 2014 ; Anderson et al, 2020 ; Shafiei et al, 2020 ; Muller et al, 2020 ) and physiological ( Sethi et al, 2017 ; Fallon et al, 2020 ) attributes of network nodes, thereby conceptually linking local and global brain organization ( Khambhati et al, 2018 ; Suárez et al, 2020 ). In such ‘annotated networks’, macroscale network architecture is thought to reflect similarity in local properties, and vice versa , such that areas with similar properties are more likely to be anatomically connected and to functionally interact with one another ( Beul et al, 2017 ; Goulas et al, 2019 ; Wei et al, 2019 ; Hilgetag et al, 2019 ).…”

Section: Discussionmentioning

confidence: 82%

“…Our results build on this literature, demonstrating that microscale and connectional hierarchies leave an indelible mark on intrinsic dynamics ( Lurie and D’Esposito, 2020 ), perhaps through variation in local excitability ( Demirtaş et al, 2019 ; Wang et al, 2019 ; Wang, 2020 ; Deco et al, 2020 ). How these patterns are related to underlying cell types and subcortical afferent input – in particular, thalamocortical feedback – is an important ongoing question ( Abeysuriya et al, 2015 ; Garrett et al, 2018 ; Shine et al, 2019 ; Wang et al, 2019 ; Muller et al, 2020 ; Paquola et al, 2020 ).…”

Section: Discussionmentioning

confidence: 99%

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Topographic gradients of intrinsic dynamics across neocortex

Shafiei

Markello

Wael

et al. 2020

eLife

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130

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The intrinsic dynamics of neuronal populations are shaped by both microscale attributes and macroscale connectome architecture. Here we comprehensively characterize the rich temporal patterns of neural activity throughout the human brain. Applying massive temporal feature extraction to regional haemodynamic activity, we systematically estimate over 6000 statistical properties of individual brain regions’ time-series across the neocortex. We identify two robust spatial gradients of intrinsic dynamics, one spanning a ventromedial-dorsolateral axis and dominated by measures of signal autocorrelation, and the other spanning a unimodal-transmodal axis and dominated by measures of dynamic range. These gradients reflect spatial patterns of gene expression, intracortical myelin and cortical thickness, as well as structural and functional network embedding. Importantly, these gradients are correlated with patterns of meta-analytic functional activation, differentiating cognitive versus affective processing and sensory versus higher-order cognitive processing. Altogether, these findings demonstrate a link between microscale and macroscale architecture, intrinsic dynamics, and cognition.

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Section: Discussionmentioning

confidence: 82%

Section: Discussionmentioning

confidence: 99%

Topographic gradients of intrinsic dynamics across neocortex

Shafiei

Markello

Wael

et al. 2020

eLife

Self Cite

130

View full text Add to dashboard Cite

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“…Notably, evaluations of several feature combinations highlighted that predictive performance was highest when including both baseline and trajectory data, and when complementing cortical and subcortical manifold features. These findings reemphasize the benefits of incorporating subcortical nodes in the characterization of large-scale cortical network organization and overall cognitive function (Alves et al, 2019; Müller et al, 2020; Shine et al, 2019).…”

Section: Discussionmentioning

confidence: 85%

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

Park

Bethlehem

Paquola

et al. 2020

Preprint

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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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“…Future studies should increase the resolution of the wiring space, which may be possible with ongoing efforts to generate robust estimates of white matter tracts from single voxels [88]. Efforts will also benefit from the incorporation of subcortical nodes, such as the thalamus, which are increasingly recognised to play major roles in cortico-cortical dynamics and have distinct cell populations projecting to specific cortical laminae [89,90]. In lieu of a gold standard for cortical wiring in humans, the present work focused on equally balanced cortical wiring features; however, supervised learning techniques could reveal their relative importance for specific tasks or scales.…”

Section: Plos Biologymentioning

confidence: 99%

A multi-scale cortical wiring space links cellular architecture and functional dynamics in the human brain

et al. 2020

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The vast net of fibres within and underneath the cortex is optimised to support the convergence of different levels of brain organisation. Here, we propose a novel coordinate system of the human cortex based on an advanced model of its connectivity. Our approach is inspired by seminal, but so far largely neglected models of cortico–cortical wiring established by postmortem anatomical studies and capitalises on cutting-edge in vivo neuroimaging and machine learning. The new model expands the currently prevailing diffusion magnetic resonance imaging (MRI) tractography approach by incorporation of additional features of cortical microstructure and cortico–cortical proximity. Studying several datasets and different parcellation schemes, we could show that our coordinate system robustly recapitulates established sensory-limbic and anterior–posterior dimensions of brain organisation. A series of validation experiments showed that the new wiring space reflects cortical microcircuit features (including pyramidal neuron depth and glial expression) and allowed for competitive simulations of functional connectivity and dynamics based on resting-state functional magnetic resonance imaging (rs-fMRI) and human intracranial electroencephalography (EEG) coherence. Our 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. Our evaluations demonstrate the cortical wiring space bridges across scales of neural organisation and can be easily translated to single individuals.

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Core and matrix thalamic sub-populations relate to spatio-temporal cortical connectivity gradients

Cited by 82 publications

References 71 publications

Topographic gradients of intrinsic dynamics across neocortex

Topographic gradients of intrinsic dynamics across neocortex

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

A multi-scale cortical wiring space links cellular architecture and functional dynamics in the human brain

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