Mapping brain asymmetry in health and disease through the <scp>ENIGMA</scp> consortium

Kong, Xiangzhen; Postema, Merel C.; Guadalupe, Tulio; Kovel, C.G.F. de; Boedhoe, Premika S.W.; Hoogman, Martine; Mathias, Samuel R.; Rooij, Daan van; Schijven, Dick; Glahn, David C.; Medland, Sarah E.; Jahanshad, Neda; Thomopoulos, Sophia I; Turner, Jessica A.; Buitelaar, Jan K.; Erp, Theo G.M. van; Franke, Barbara; Fisher, Simon E.; Heuvel, Odile A. van den; Schmaal, Lianne; Thompson, Paul M.; Francks, Clyde

doi:10.1002/hbm.25033

Cited by 132 publications

(139 citation statements)

References 138 publications

(162 reference statements)

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“…Thus, loss of thickness asymmetry may be more relevant for advanced cognitive decline -such as that associated with AD -but less sensitive to individual differences in cognitive decline trajectories across the healthy adult lifespan. Although we note that alternative tests such as cognitive speed measures may be better suited than task accuracy for assessing asymmetry-cognition relationships, our results suggest that asymmetry-change may be unlikely to be a sensitive marker for age-related decline at the individual level (similar conclusions have recently been drawn in relation to asymmetry in other contexts 68 ). This is also evidenced by the fact that our large longitudinal sample sizes were needed to expose small-to-medium effects that nevertheless translated to consistent gradual changes in asymmetry across adult lifespan samples.…”

Section: Discussionsupporting

confidence: 51%

Asymmetric thinning of the cerebral cortex across the adult lifespan is accelerated in Alzheimer’s Disease

Roe

Vidal-Piñeiro

Sørensen

et al. 2020

Preprint

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Normal aging and Alzheimer's Disease (AD) are accompanied by large-scale alterations in brain organization that undermine brain function. Although hemispheric asymmetry is a global organizing feature of cortex thought to promote brain efficiency, current descriptions of cortical thinning in aging and AD have largely overlooked cortical asymmetry. Consequently, the foundational question of whether and where the cerebral hemispheres change at different rates in aging and AD remains open. First, applying vertex-wise data-driven clustering in a longitudinal discovery sample (aged 20-89; 2577 observations; 1851 longitudinal) we identified cortical regions exhibiting similar age-trajectories of asymmetry across the adult lifespan. Next, we sought replication in 4 independent longitudinal aging cohorts. We show that higher-order regions of cortex that exhibit pronounced asymmetry at age ~20 also show asymmetry change in aging. Results revealed that both leftward and rightward asymmetry is progressively lost on a similar time-scale across adult life. Hence, faster thinning of the (previously) thicker homotopic hemisphere is a feature of aging. This simple organizational principle showed high consistency across multiple aging cohorts in the Lifebrain consortium, and both the topological patterns and temporal dynamics of asymmetry-loss were markedly similar across replicating samples. Finally, we show that regions exhibiting gradual asymmetry-loss over healthy adult life exhibit faster asymmetry-change in AD.Overall, our results suggest a system-wide breakdown in the adaptive asymmetric organization of cortex across adult life which is further accelerated in AD, and may implicate thickness asymmetry as a viable marker for declining hemispheric specialization in aging and AD. The brain becomes progressively disorganized with age, and brain alterations accelerated in Alzheimer's disease may occur gradually over the lifespan. Although hemispheric asymmetry aids efficient network organization, efforts to identify structural markers of age-related decline have largely overlooked cortical asymmetry. Here we show the hemisphere that is thicker when younger, thins faster. This leads to progressive system-wide loss of regional thickness asymmetry across life. In multiple aging cohorts, asymmetry-loss showed high reproducibility topologically across cortex and similar timing-of-change in aging. Asymmetry-change was further accelerated in AD. Our findings uncover a new principle of brain aging -thicker homotopic cortex thins faster -and suggest we may have unveiled a structural marker for a widely-hypothesized decline in hemispheric specialization in aging and AD.

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Section: Discussionsupporting

confidence: 51%

Asymmetric thinning of the cerebral cortex across the adult lifespan is accelerated in Alzheimer’s Disease

Roe

Vidal-Piñeiro

Sørensen

et al. 2020

Preprint

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“…The Davi130 parcellation was realized by utilizing macroscopic gyral and sulcal features such as peaks, fundi, and bends to represent the chimpanzee brain in a reduced dimensional space based on macro-anatomical landmarks. Despite the evidence that true microanatomical borders between brain areas rarely coincide with macro-anatomical patterns (Amunts and Zilles 2015), macroscopic brain parcellations like Desikan-Killany human atlas (Desikan et al 2006) have successfully been utilized in many studies furthering our understanding of brain structure, function, and disease (Kong et al 2020;van den Heuvel et al 2020). The Davi130 parcellation of the chimpanzee brain serves two main purposes.…”

Section: Discussionmentioning

confidence: 99%

Chimpanzee brain morphometry utilizing standardized MRI preprocessing and macroanatomical annotations

Vickery

Hopkins

Sherwood

et al. 2020

eLife

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Chimpanzees are among the closest living relatives to humans and, as such, provide a crucial comparative model for investigating primate brain evolution. In recent years, human brain mapping has strongly benefited from enhanced computational models and image processing pipelines that could also improve data analyses in animals by using species-specific templates. In this study, we use structural MRI data from the National Chimpanzee Brain Resource (NCBR) to develop the chimpanzee brain reference template Juna.Chimp for spatial registration and the macro-anatomical brain parcellation Davi130 for standardized whole-brain analysis. Additionally, we introduce a ready-to-use image processing pipeline built upon the CAT12 toolbox in SPM12, implementing a standard human image preprocessing framework in chimpanzees. Applying this approach to data from 194 subjects, we find strong evidence for human-like age-related gray matter atrophy in multiple regions of the chimpanzee brain, as well as, a general rightward asymmetry in brain regions.

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“…Our approach is akin to studying seismic waves of earthquakes with different wave frequencies at the global tectonic scale, instead of focusing on a particular city. The ability to assess shape along a spectrum of spatial scales is important, since brain asymmetry is a multidimensional and multivariate phenotype (3,13,45).…”

Section: Identifiability Of Cortical Shape Asymmetry Is Maximal At Coarse Scalesmentioning

confidence: 99%

“…Similarly, some studies have found associations between cerebral asymmetry and handedness (8,14,33), with others reporting no such effect (10,11,28,32,(34)(35)(36). Some of these inconsistencies may arise from the disparate methodologies and the heterogeneous nature of the brain asymmetries across the population (7,10,(12)(13)(14)(15). There is often considerable individual variability around population means, with many people often showing little or even reversed asymmetries relative to the group average (3,12,16,37).…”

Section: Introductionmentioning

confidence: 99%

The individuality of shape asymmetries of the human cerebral cortex

Chen

Arnatkevičiūtė

McTavish

et al. 2021

Preprint

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Asymmetries of the cerebral cortex are found across diverse phyla and occur at multiple spatial scales, from the global morphology of the two hemispheres to fine-grained sulcal and gyral anatomy. Cortical asymmetries are particularly pronounced in humans and have important implications for brain function and disease. However, most studies conflate asymmetries in regional size and shape and only consider effects at fairly fine-grained resolutions, such as image voxels or a priori regions-of-interest. As such, whether asymmetries are preferentially expressed at specific spatial resolutions over others remains unclear. Here, we apply a spectral shape analysis to magnetic resonance imaging (MRI) data from three independent samples to derive a multiscale description of asymmetries in cortical shape that is distinct from regional size-related descriptors such as volume or thickness. We show that our proposed shape asymmetry signature (SAS) is a highly individualized feature, akin to a cortical fingerprint, that more accurately identifies individuals than size-based descriptors or measures of inter-regional functional coupling of brain activity. Notably, individual identifiability is optimal at coarse spatial scales (~37 mm wavelength), and shape asymmetries at specific scales show differences between males and females but are unrelated to the handedness. We further demonstrate that while unihemispheric shape descriptors show significant heritability at coarse scales, the SAS are determined primarily by unique environmental effects across all scales considered. Our findings thus identify coarse-scale scale asymmetries of cortical shape as being highly unique to individuals, sexually dimorphic, and largely driven by stochastic environmental influences.

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Mapping brain asymmetry in health and disease through the ENIGMA consortium

Abstract: Left-right asymmetry of the human brain is one of its cardinal features, and also a complex, multivariate trait. Decades of research have suggested that brain asymmetry

Cited by 132 publications

References 138 publications

Asymmetric thinning of the cerebral cortex across the adult lifespan is accelerated in Alzheimer’s Disease

Asymmetric thinning of the cerebral cortex across the adult lifespan is accelerated in Alzheimer’s Disease

Chimpanzee brain morphometry utilizing standardized MRI preprocessing and macroanatomical annotations

The individuality of shape asymmetries of the human cerebral cortex

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