Anatomical and diffusion MRI brain atlases of the fetal rhesus macaque brain at 85, 110 and 135 days gestation

Liu, Zheng; Wang, Xiaojie; Newman, Natali; Grant, Kathleen A.; Studholme, Colin; Kroenke, Christopher D.

doi:10.1016/j.neuroimage.2019.116310

Cited by 19 publications

(15 citation statements)

References 47 publications

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“…4 A ), long-distance cortico-cortical connections reach the subplate and/or cortical plate beginning ∼E106 for area V4 ( 87 ) and ∼E108 for V1-V2 ( 90 ). This overlaps with the main gyrification period (∼E100 to ∼E135) ( 91 – 93 ). Axons tend to run in parallel in the developing white matter, forming numerous long-distance fiber tracts.…”

Section: Early Forebrain Developmentmentioning

confidence: 81%

A 2020 view of tension-based cortical morphogenesis

Essen

2020

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

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Mechanical tension along the length of axons, dendrites, and glial processes has been proposed as a major contributor to morphogenesis throughout the nervous system [D. C. Van Essen, Nature 385, 313–318 (1997)]. Tension-based morphogenesis (TBM) is a conceptually simple and general hypothesis based on physical forces that help shape all living things. Moreover, if each axon and dendrite strive to shorten while preserving connectivity, aggregate wiring length would remain low. TBM can explain key aspects of how the cerebral and cerebellar cortices remain thin, expand in surface area, and acquire their distinctive folds. This article reviews progress since 1997 relevant to TBM and other candidate morphogenetic mechanisms. At a cellular level, studies of diverse cell types in vitro and in vivo demonstrate that tension plays a major role in many developmental events. At a tissue level, I propose a differential expansion sandwich plus (DES+) revision to the original TBM model for cerebral cortical expansion and folding. It invokes tangential tension and “sulcal zipping” forces along the outer cortical margin as well as tension in the white matter core, together competing against radially biased tension in the cortical gray matter. Evidence for and against the DES+ model is discussed, and experiments are proposed to address key tenets of the DES+ model. For cerebellar cortex, a cerebellar multilayer sandwich (CMS) model is proposed that can account for many distinctive features, including its unique, accordion-like folding in the adult, and experiments are proposed to address its specific tenets.

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Section: Early Forebrain Developmentmentioning

confidence: 81%

A 2020 view of tension-based cortical morphogenesis

Essen

2020

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

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“…While GM/WM composition differences between male and female brains are described for humans (Allen et al, 2003), no significant difference was reported in sheep (Nitzsche et al, 2015). Thus the exact magnitude of this limitation is uncertain in our study; rather, other factors such as age appear to play a bigger role in determining important morphological differences (Nitzsche et al, 2015;Johnson et al, 2019;Liu et al, 2020). Finally, although our template is representative of the inter-individual variation found amongst the adult Yucatan micropig population, this variation is likely different for other pig breeds, including other miniature breeds.…”

Section: Limitationsmentioning

confidence: 54%

In vivo Population Averaged Stereotaxic T2w MRI Brain Template for the Adult Yucatan Micropig

et al. 2020

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“…White Matter Characterization. Similar to volumetric estimation, FA maps of individual fetal brains were registered to age-specific FA templates of rhesus macaque fetal brains (23). White matter ROIs featured in the atlas were then propagated back to individual FA maps and FA values were averaged within each ROI for each fetal brain.…”

Section: Methodsmentioning

confidence: 99%

“…These are the cortical plate, the developing white matter (termed subplate and intermediate zone at G85), the striatum, the thalamus, the brainstem, and the cerebellum. In addition, FA within 8 white matter ROIs were analyzed in the G110 cohort and 11 white matter ROIs in the G135 cohort (23). Within each of the six groups (ethanol-exposed and control groups at three gestational ages), the distributions of all brain region volumes and all FA values were found to be normally distributed (Shapiro-Wilk test, P > 0.05).…”

Section: Methodsmentioning

confidence: 99%

“…In order to compare overall brain sizes, age-appropriate rhesus macaque template images were used, which have each been segmented into a common set of six brain regions (23). The total brain volume and the volumes of each brain region were determined following nonlinear registration of the segmented template to each fetus' T 2 -weighted image.…”

Section: (B and C)mentioning

confidence: 99%

See 1 more Smart Citation

In utero MRI identifies consequences of early-gestation alcohol drinking on fetal brain development in rhesus macaques

Wang

Carlson

Studholme

et al. 2020

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

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One factor that contributes to the high prevalence of fetal alcohol spectrum disorder (FASD) is binge-like consumption of alcohol before pregnancy awareness. It is known that treatments are more effective with early recognition of FASD. Recent advances in retrospective motion correction for the reconstruction of three-dimensional (3D) fetal brain MRI have led to significant improvements in the quality and resolution of anatomical and diffusion MRI of the fetal brain. Here, a rhesus macaque model of FASD, involving oral self-administration of 1.5 g/kg ethanol per day beginning prior to pregnancy and extending through the first 60 d of a 168-d gestational term, was utilized to determine whether fetal MRI could detect alcohol-induced abnormalities in brain development. This approach revealed differences between ethanol-exposed and control fetuses at gestation day 135 (G135), but not G110 or G85. At G135, ethanol-exposed fetuses had reduced brainstem and cerebellum volume and water diffusion anisotropy in several white matter tracts, compared to controls. Ex vivo electrophysiological recordings performed on fetal brain tissue obtained immediately following MRI demonstrated that the structural abnormalities observed at G135 are of functional significance. Specifically, spontaneous excitatory postsynaptic current amplitudes measured from individual neurons in the primary somatosensory cortex and putamen strongly correlated with diffusion anisotropy in the white matter tracts that connect these structures. These findings demonstrate that exposure to ethanol early in gestation perturbs development of brain regions associated with motor control in a manner that is detectable with fetal MRI.

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Anatomical and diffusion MRI brain atlases of the fetal rhesus macaque brain at 85, 110 and 135 days gestation

Cited by 19 publications

References 47 publications

A 2020 view of tension-based cortical morphogenesis

A 2020 view of tension-based cortical morphogenesis

In vivo Population Averaged Stereotaxic T2w MRI Brain Template for the Adult Yucatan Micropig

In utero MRI identifies consequences of early-gestation alcohol drinking on fetal brain development in rhesus macaques

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