Gyrification of the cerebral cortex requires FGF signaling in the mammalian brain

Matsumoto, Naoyuki; Shinmyo, Yohei; Ichikawa, Yoshie; Kawasaki, Hiroshi

doi:10.7554/elife.29285

Cited by 65 publications

(61 citation statements)

References 49 publications

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“…The cortical folding has been hypothesized to be a result of the regional neuronal differentiation and migration (Zilles, Armstrong, Schleicher, & Kretschmann, ), and mechanical tension by the underlying axonal connections (Van Essen, ). More recent research revealed that an increased number of neural progenitors in the subventricular zone are essential for gyrification of the cortical cortex (Matsumoto, Shinmyo, Ichikawa, & Kawasaki, ). The GI is an index representing the degree of gyrification; the ratio of the contour of the pial surface against the outer contour of the cerebral cortex, representing the degree of cortical folding (Matsuda & Ohi, ).…”

Section: Discussionmentioning

confidence: 99%

Brain morphological analysis in PTEN hamartoma tumor syndrome

Shiohama

Levman

Vasung

et al. 2020

American J of Med Genetics Pt A

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PTEN hamartoma tumor syndrome (PHTS) is a spectrum of hereditary cancer syndromes caused by germline mutations in PTEN. PHTS is of high interest, because of its high rate of neurological comorbidities including macrocephaly, autism spectrum disorder, and intellectual dysfunction. Since detailed brain morphology and connectivity of PHTS remain unclear, we quantitatively evaluated brain magnetic resonance imaging (MRI) in PHTS. Sixteen structural T1-weighted and 9 diffusion-weighted MR images from 12 PHTS patients and neurotypical controls were used for structural and high-angular resolution diffusion MRI (HARDI) tractography analyses. Megacorpus callosum was observed in 75%, polymicrogyria in 33%, periventricular white matter lesions in 83%, and heterotopia in 17% of the PHTS participants. While gyrification index and hemispheric cortical thickness showed no significant differences between the two groups, significantly increased global and regional brain volumes, and regionally thicker cortices in PHTS participants were observed. HARDI tractography showed increased volume and length of callosal pathways, increased volume of the arcuate fasciculi (AF), and increased length of the bilateral inferior longitudinal fasciculi (ILF), bilateral inferior fronto-occipital fasciculi (IFOF), and bilateral uncinate fasciculus. A decrease in fractional anisotropy and an increased in apparent diffusion coefficient values of the AF, left ILF, and left IFOF in PHTS. K E Y W O R D SHARDI, mega corpus callosum, megalencephaly, PTEN hamartoma tumor syndrome, structural brain MRI

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Section: Discussionmentioning

confidence: 99%

Brain morphological analysis in PTEN hamartoma tumor syndrome

Shiohama

Levman

Vasung

et al. 2020

American J of Med Genetics Pt A

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“…Combination of in situ hybridization and immunostaining was described previously (Matsumoto et al, 2017). Briefly, after hybridization, sections were incubated with mouse anti-Pax6 antibody (Abcam; RRID:AB_1566562) and rabbit anti-Tbr2 antibody (Abcam; RRID: AB_778267).…”

Section: Figurementioning

confidence: 99%

“…RNA probes for mouse Fgfr1, Fgfr2, and Fgfr3 were described previously (Matsumoto et al, 2017). To make RNA probes for mouse Etv5 and Spry2, cDNA fragments were amplified with RT-PCR using the following primers.…”

Section: Figurementioning

confidence: 99%

FGF Signaling Directs the Cell Fate Switch from Neurons to Astrocytes in the Developing Mouse Cerebral Cortex

et al. 2019

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During mammalian neocortical development, neural precursor cells generate neurons first and astrocytes later. The cell fate switch from neurons to astrocytes is a key process generating proper numbers of neurons and astrocytes. Although the intracellular mechanisms regulating this cell fate switch have been well characterized, extracellular regulators are still largely unknown. Here, we uncovered that fibroblast growth factor (FGF) regulates the cell fate switch from neurons to astrocytes in the developing cerebral cortex using mice of both sexes. We found that the FGF signaling pathway is activated in radial glial cells of the ventricular zone at time points corresponding to the switch in cell fate. Our loss-and gain-of-function studies using in utero electroporation indicate that activation of FGF signaling is necessary and sufficient to change cell fates from neurons to astrocytes. We further found that the FGF-induced neuron-astrocyte cell fate switch is mediated by the MAPK pathway. These results indicate that FGF is a critical extracellular regulator of the cell fate switch from neurons to astrocytes in the mammalian cerebral cortex.Although the intracellular mechanisms regulating the neuron-astrocyte cell fate switch in the mammalian cerebral cortex during development have been well studied, their upstream extracellular regulators remain unknown. By using in utero electroporation, our study provides in vivo data showing that activation of FGF signaling is necessary and sufficient for changing cell fates from neurons to astrocytes. Manipulation of FGF signaling activity led to drastic changes in the numbers of neurons and astrocytes. These results indicate that FGF is a key extracellular regulator determining the numbers of neurons and astrocytes in the mammalian cerebral cortex, and is indispensable for the establishment of appropriate neural circuitry.

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“…The differential growth across the cortex, the migration of neurons along radial glia, and/or the differential expansion of upper versus lower layer neurons are a few proposed mechanisms generating variation in cortical folding between species (Richman et al, 1975;Van Essen, 1997;Toro and Burnod, 2005;Xu et al, 2010;Chen et al, 2013;Striedter et al, 2015;Fernández et al, 2016;Tallinen et al, 2016;Razavi et al, 2017). Modifications to neurogenetic programs are well-documented sources of variation across species, and experimental manipulations of cell proliferation during development impact cortical composition, as well as cortical folding (Dyer et al, 2009;Clowry et al, 2010;Striedter, 2008, 2011;Charvet et al, 2017ab;Lewitus et al, 2013;McGowan et al, 2012McGowan et al, , 2013Nonaka-Kinoshita et al, 2013;Borrell and Götz, 2014;Otani et al, 2016;Tallinen et al, 2016;Toda et al, 2016;Matsumoto et al, 2017;Shinmyo et al, 2017;de Juan Romero and Borrell, 2017). We suggest that the differential composition of neurons across the depth of the cortex may cause major differences in white matter tension between species.…”

Section: Cortico-cortical Projections and Gyrificationmentioning

confidence: 99%

Evolution of connections and cell types: integrating diffusion MR tractography with gene expression data highlights increased cortico-cortical projections in primates

Charvet

Kabaria

Takahashi

2018

Preprint

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Diffusion MR tractography permits investigating the three-dimensional structure of cortical pathways as interwoven paths across the entire brain. We use high-resolution scans from diffusion spectrum imaging and high angular resolution diffusion imaging to investigate the evolution of cortical pathways within the euarchontoglire (i.e., primates, rodents) lineage. More specifically, we compare cortical fiber pathways between macaques (Macaca mulatta), marmosets (Callithrix jachus), and rodents (mice, Mus musculus). We integrate these observations with comparative analyses of Neurofilament heavy polypeptide (NEFH) expression across the cortex of mice and primates. We chose these species because their phylogenetic position serves to trace the early evolutionary history of the human brain. Our comparative analysis from diffusion MR tractography and NEFH expression demonstrates that the examined primates deviate from mice in possessing increased longrange cross-cortical projections, many of which course across the anterior to posterior axis of the cortex. Our study shows that integrating gene expression data with diffusion MR data is an effective approach in identifying variation in connectivity patterns between species. The expansion of cortico-cortical pathways and increased anterior to posterior cortical integration can be traced back to an extension of neurogenetic schedules during development in primates.

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Gyrification of the cerebral cortex requires FGF signaling in the mammalian brain

Cited by 65 publications

References 49 publications

Brain morphological analysis in PTEN hamartoma tumor syndrome

Brain morphological analysis in PTEN hamartoma tumor syndrome

FGF Signaling Directs the Cell Fate Switch from Neurons to Astrocytes in the Developing Mouse Cerebral Cortex

Evolution of connections and cell types: integrating diffusion MR tractography with gene expression data highlights increased cortico-cortical projections in primates

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