White matter volume and white/gray matter ratio in mammalian species as a consequence of the universal scaling of cortical folding

Mota, Bruno; Santos, Sandra Esmeralda Dos; Ventura-Antunes, Lissa; Jardim-Messeder, Débora; Neves, Kleber; Kazu, Rodrigo S.; Noctor, Stephen C.; Lambert, Kelly G.; Bertelsen, Mads F.; Manger, Paul R.; Sherwood, Chet C.; Kaas, Jon H.; Herculano‐Houzel, Suzana

doi:10.1073/pnas.1716956116

Cited by 50 publications

(57 citation statements)

References 27 publications

(31 reference statements)

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“…It should however be noted that other reports seem to be at odds with these results, suggesting a significant vulnerability of the human connectome against targeted attacks in human networks (see 32 for a recent overview on the topic). Whether these discrepancies reflect modality-and resolution-related discrepancies, or a lower proportion of long-range integrative fibers in rodents owing to evolutionary scaling of white/grey matter ratio 53 , remains to be established.…”

Section: Discussionmentioning

confidence: 99%

Network structure of the mouse brain connectome with voxel resolution

Coletta

Pagani

Whitesell

et al. 2020

Preprint

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Fine-grained descriptions of brain connectivity are fundamental for understanding how neural information is processed and relayed across spatial scales. Prior investigations of the mouse brain connectome have employed discrete anatomical parcellations, limiting spatial resolution and potentially concealing network attributes critical to the organization of the mammalian connectome.Here we provide a voxel-level description of the network and hierarchical structure of the directed mouse connectome, unconstrained by regional partitioning. We show that integrative hub regions can be directionally segregated into neural sinks and sources, defining a hierarchical axis. We describe a set of structural communities that spatially reconstitute previously described fMRI networks of the mouse brain, and document that neuromodulatory nuclei are strategically wired as critical orchestrators of inter-modular and network communicability. Notably, like in primates, the directed mouse connectome is organized along two superimposed cortical gradients reflecting unimodaltransmodal functional processing and a modality-specific sensorimotor axis. These structural features can be related to patterns of intralaminar connectivity and to the spatial topography of dynamic fMRI brain states, respectively. Together, our results reveal a high-resolution structural scaffold linking mesoscale connectome topography to its macroscale functional organization, and create opportunities for identifying targets of interventions to modulate brain function in a physiologicallyaccessible species.

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Section: Discussionmentioning

confidence: 99%

Network structure of the mouse brain connectome with voxel resolution

Coletta

Pagani

Whitesell

et al. 2020

Preprint

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“…With increasing brain size, subcortical structures (brainstem, thalamus, basal ganglia) increase more slowly in volume than does cerebral cortex (8,10,11). Subcortical white matter, on the other hand, increases more steeply than does cortical gray matter volume (12). However, increases in cortical volume are reflected mainly in an expanded surface area, because cortical thickness increases with a very shallow slope (13,14).…”

Section: Brain Size and Cortical Convolutionsmentioning

confidence: 99%

Cerebral cortical folding, parcellation, and connectivity in humans, nonhuman primates, and mice

Essen

Donahue

Coalson

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

160

127

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Advances in neuroimaging and neuroanatomy have yielded major insights concerning fundamental principles of cortical organization and evolution, thus speaking to how well different species serve as models for human brain function in health and disease. Here, we focus on cortical folding, parcellation, and connectivity in mice, marmosets, macaques, and humans. Cortical folding patterns vary dramatically across species, and individual variability in cortical folding increases with cortical surface area. Such issues are best analyzed using surface-based approaches that respect the topology of the cortical sheet. Many aspects of cortical organization can be revealed using 1 type of information (modality) at a time, such as maps of cortical myelin content. However, accurate delineation of the entire mosaic of cortical areas requires a multimodal approach using information about function, architecture, connectivity, and topographic organization. Comparisons across the 4 aforementioned species reveal dramatic differences in the total number and arrangement of cortical areas, particularly between rodents and primates. Hemispheric variability and bilateral asymmetry are most pronounced in humans, which we evaluated using a high-quality multimodal parcellation of hundreds of individuals. Asymmetries include modest differences in areal size but not in areal identity. Analyses of cortical connectivity using anatomical tracers reveal highly distributed connectivity and a wide range of connection weights in monkeys and mice; indirect measures using functional MRI suggest a similar pattern in humans. Altogether, a multifaceted but integrated approach to exploring cortical organization in primate and nonprimate species provides complementary advantages and perspectives. macaque | marmoset | neuroanatomy | cerebral cortex | neuroimaging C erebral cortex is the dominant structure of the mammalian brain and is implicated in a wide range of sensory, motor, cognitive, and emotional functions. Despite wide variations across species in size and morphological complexity, there are fundamental commonalities in cortical structure and function across all mammals. Most notably, cerebral cortex is a thin, layered sheet of gray matter containing a mosaic of cortical areas that differ in architecture, connectivity, topography (maps of sensory or motor domains), and/or function (1, 2).Our ability to investigate how cerebral cortex is organized and how it "works" has been greatly enhanced in recent decades by a growing arsenal of powerful and complementary experimental methods, both invasive (mainly applicable to animal models) and noninvasive (widely applicable to humans). Invasive anatomical, electrophysiological, and optical methods are available over a wide range of spatial scales (micro-, meso-, and macroscopic), and they provide a remarkably rich and diverse range of information. Many of these tools require complex genetic manipulations and hence are limited to genetically tractable species, especially the mouse but more recently also the m...

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“…There are also a number of studies in which the volumes of the white and gray matters are evaluated. The relative volume of the gray matter decreases significantly with increasing body size and increasing number of neurons, and slopes and elevations differ between groups 79 – 81 . The relative volume of the gray matter in vertebrates varies between species within a very wide range, from 93% in the mouse Mus musculus to 66% in humans and to 50% in the elephant Loxodonta africana 81 .…”

Section: Resultsmentioning

confidence: 96%

Constant neuropilar ratio in the insect brain

Polilov

Makarova

2020

Sci Rep

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Revealing scaling rules is necessary for understanding the morphology, physiology and evolution of living systems. Studies of animal brains have revealed both general patterns, such as Haller's rule, and patterns specific for certain animal taxa. However, large-scale studies aimed at studying the ratio of the entire neuropil and the cell body rind in the insect brain have never been performed. Here we performed morphometric study of the adult brain in 37 insect species of 26 families and ten orders, ranging in volume from the smallest to the largest by a factor of more than 4,000,000, and show that all studied insects display a similar ratio of the volume of the neuropil to the cell body rind, 3:2. Allometric analysis for all insects shows that the ratio of the volume of the neuropil to the volume of the brain changes strictly isometrically. Analyses within particular taxa, size groups, and metamorphosis types also reveal no significant differences in the relative volume of the neuropil; isometry is observed in all cases. Thus, we establish a new scaling rule, according to which the relative volume of the entire neuropil in insect brain averages 60% and remains constant.

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White matter volume and white/gray matter ratio in mammalian species as a consequence of the universal scaling of cortical folding

Cited by 50 publications

References 27 publications

Network structure of the mouse brain connectome with voxel resolution

Network structure of the mouse brain connectome with voxel resolution

Cerebral cortical folding, parcellation, and connectivity in humans, nonhuman primates, and mice

Constant neuropilar ratio in the insect brain

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