[en] In the middle of March 2019, a group of scientists and clinicians (as well as those who wear both hats) gathered in the green campus of the Weizmann Institute of Science to share recent scientific findings, to establish collaborations, and to discuss future directions for better diagnosis, etiology modeling and treatment of brain malformations. One hundred fifty scientists from twenty-two countries took part in this meeting. Thirty-eight talks were presented and as many as twenty-five posters were displayed. This review is aimed at presenting some of the highlights that the audience was exposed to during the three-day meeting.
Disciplines :
Neurology
Author, co-author :
Sapir, Tamar
Barakat, Tahsin Stefan
Paredes, Mercedes F.
Lerman-Sagie, Tally
Aronica, Eleonora
Klonowski, Wlodzimierz
Nguyen, Laurent ; Université de Liège - ULiège > Stem Cells-Molecular Regulation of Neurogenesis
Ben Zeev, Bruria
Bahi-Buisson, Nadia
Leventer, Richard
Rachmian, Noa
Reiner, Orly
Language :
English
Title :
Building Bridges Between the Clinic and the Laboratory: A Meeting Review - Brain Malformations: A Roadmap for Future Research.
Arlotta P., Pasca S. P., (2019). Cell diversity in the human cerebral cortex: from the embryo to brain organoids. Curr. Opin. Neurobiol. 56 194–198. 10.1016/j.conb.2019.03.001 31051421
Baldassari S., Ribierre T., Marsan E., Adle-Biassette H., Ferrand-Sorbets S., Dorfmüller G., (2019). Dissecting the genetic basis of focal cortical dysplasia: a large cohort study. Acta Neuropathol. 10.1007/s00401-019-02061-5 [Epub ahead of print]. 31444548
Barakat T. S., Halbritter F., Zhang M., Rendeiro A. F., Perenthaler E., Bock C., (2018). Functional dissection of the enhancer repertoire in human embryonic stem cells. Cell Stem Cell 23 e278. 10.1016/j.stem.2018.06.014 30033119
Barkovich A. J., Dobyns W. B., Guerrini R., (2015). Malformations of cortical development and epilepsy. Cold Spring Harb. Perspect. Med. 5:a022392. 10.1101/cshperspect.a022392 25934463
Barkovich A. J., Guerrini R., Kuzniecky R. I., Jackson G. D., Dobyns W. B., (2012). A developmental and genetic classification for malformations of cortical development: update 2012. Brain 135 1348–1369. 10.1093/brain/aws019 22427329
Baybis M., Yu J., Lee A., Golden J. A., Weiner H., McKhann G., II (2004). mTOR cascade activation distinguishes tubers from focal cortical dysplasia. Ann. Neurol. 56 478–487. 10.1002/ana.20211 15455405
Bernier R., Golzio C., Xiong B., Stessman H. A., Coe B. P., Penn O., (2014). Disruptive CHD8 mutations define a subtype of autism early in development. Cell 158 263–276. 10.1016/j.cell.2014.06.017 24998929
Bershteyn M., Nowakowski T. J., Pollen A. A., Di Lullo E., Nene A., Wynshaw-Boris A., (2017). Human iPSC-derived cerebral organoids model cellular features of lissencephaly and reveal prolonged mitosis of outer radial glia. Cell Stem Cell 20:e434. 10.1016/j.stem.2016.12.007 28111201
Betizeau M., Cortay V., Patti D., Pfister S., Gautier E., Bellemin-Menard A., (2013). Precursor diversity and complexity of lineage relationships in the outer subventricular zone of the primate. Neuron 80 442–457. 10.1016/j.neuron.2013.09.032 24139044
Blumcke I., Thom M., Aronica E., Armstrong D. D., Vinters H. V., Palmini A., (2011). The clinicopathologic spectrum of focal cortical dysplasias: a consensus classification proposed by an ad hoc Task Force of the ILAE diagnostic methods commission. Epilepsia 52 158–174. 10.1111/j.1528-1167.2010.02777.x 21219302
Cai X., Evrony G. D., Lehmann H. S., Elhosary P. C., Mehta B. K., Poduri A., (2015). Single-cell, genome-wide sequencing identifies clonal somatic copy-number variation in the human brain. Cell Rep. 10:645. 10.1016/j.celrep.2015.01.028 25832109
Cappello S., Gray M. J., Badouel C., Lange S., Einsiedler M., Srour M., (2013). Mutations in genes encoding the cadherin receptor-ligand pair DCHS1 and FAT4 disrupt cerebral cortical development. Nat. Genet. 45 1300–1308. 10.1038/ng.2765 24056717
Carabalona A., Beguin S., Pallesi-Pocachard E., Buhler E., Pellegrino C., Arnaud K., (2012). A glial origin for periventricular nodular heterotopia caused by impaired expression of filamin-A. Hum. Mol. Genet. 21 1004–1017. 10.1093/hmg/ddr531 22076441
Cardenas A., Villalba A., de Juan Romero C., Pico E., Kyrousi C., Tzika A. C., (2018). Evolution of cortical neurogenesis in amniotes controlled by robo signaling levels. Cell 174:590-606.e521. 10.1016/j.cell.2018.06.007 29961574
Cederquist G. Y., Asciolla J. J., Tchieu J., Walsh R. M., Cornacchia D., Resh M. D., (2019). Specification of positional identity in forebrain organoids. Nat. Biotechnol. 37 436–444. 10.1038/s41587-019-0085-3 30936566
Crino P. B., (2015). mTOR signaling in epilepsy: insights from malformations of cortical development. Cold Spring Harb. Perspect. Med. 5:a022442. 10.1101/cshperspect.a022442 25833943
Crino P. B., Nathanson K. L., Henske E. P., (2006). The tuberous sclerosis complex. N. Engl. J. Med. 355 1345–1356.
Curatolo P., Moavero R., van Scheppingen J., Aronica E., (2018). mTOR dysregulation and tuberous sclerosis-related epilepsy. Expert Rev. Neurother. 18 185–201. 10.1080/14737175.2018.1428562 29338461
Cuvertino S., Stuart H. M., Chandler K. E., Roberts N. A., Armstrong R., Bernardini L., (2017). ACTB Loss-of-function mutations result in a pleiotropic developmental disorder. Am. J. Hum. Genet. 101 1021–1033. 10.1016/j.ajhg.2017.11.006 29220674
de Wit M. C., Lequin M. H., de Coo I. F., Brusse E., Halley D. J., van de Graaf R., (2008). Cortical brain malformations: effect of clinical, neuroradiological, and modern genetic classification. Arch. Neurol. 65 358–366. 10.1001/archneur.65.3.358 18332248
Dehay C., Kennedy H., Kosik K. S., (2015). The outer subventricular zone and primate-specific cortical complexification. Neuron 85 683–694. 10.1016/j.neuron.2014.12.060 25695268
Di Lullo E., Kriegstein A. R., (2017). The use of brain organoids to investigate neural development and disease. Nat. Rev. Neurosci. 18 573–584. 10.1038/nrn.2017.107 28878372
Dibbens L. M., de Vries B., Donatello S., Heron S. E., Hodgson B. L., Chintawar S., (2013). Mutations in DEPDC5 cause familial focal epilepsy with variable foci. Nat. Genet. 45 546–551. 10.1038/ng.2599 23542697
Dobyns W. B., Aldinger K. A., Ishak G. E., Mirzaa G. M., Timms A. E., Grout M. E., (2018). MACF1 mutations encoding highly conserved zinc-binding residues of the gar domain cause defects in neuronal migration and axon guidance. Am. J. Hum. Genet. 103 1009–1021. 10.1016/j.ajhg.2018.10.019 30471716
Eiraku M., Watanabe K., Matsuo-Takasaki M., Kawada M., Yonemura S., Matsumura M., (2008). Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 3 519–532. 10.1016/j.stem.2008.09.002 18983967
Evrony G. D., Lee E., Park P. J., Walsh C. A., (2016). Resolving rates of mutation in the brain using single-neuron genomics. eLife 5:e12966. 10.7554/eLife.12966 26901440
Fietz S. A., Lachmann R., Brandl H., Kircher M., Samusik N., Schroder R., (2012). Transcriptomes of germinal zones of human and mouse fetal neocortex suggest a role of extracellular matrix in progenitor self-renewal. Proc. Natl. Acad. Sci. U.S.A. 109 11836–11841. 10.1073/pnas.1209647109 22753484
Florio M., Albert M., Taverna E., Namba T., Brandl H., Lewitus E., (2015). Human-specific gene ARHGAP11B promotes basal progenitor amplification and neocortex expansion. Science 347 1465–1470. 10.1126/science.aaa1975 25721503
Florio M., Namba T., Paabo S., Hiller M., Huttner W. B., (2016). A single splice site mutation in human-specific ARHGAP11B causes basal progenitor amplification. Sci. Adv. 2:e1601941. 10.1126/sciadv.1601941 27957544
Foesleitner O., Nenning K. H., Traub-Weidinger T., Feucht M., Bonelli S., Czech T., (2018). Assessing corticospinal tract asymmetry in unilateral polymicrogyria. AJNR Am. J. Neuroradiol. 39 1530–1535. 10.3174/ajnr.A5715 29954815
Giandomenico S. L., Mierau S. B., Gibbons G. M., Wenger L. M. D., Masullo L., Sit T., (2019). Cerebral organoids at the air-liquid interface generate diverse nerve tracts with functional output. Nat. Neurosci. 22 669–679. 10.1038/s41593-019-0350-2 30886407
Guerrini R., (2005). Genetic malformations of the cerebral cortex and epilepsy. Epilepsia 46(Suppl. 1), 32–37. 10.1111/j.0013-9580.2005.461010.x 15816977
Guerrini R., (2006). Epilepsy in children. Lancet 367 499–524. 16473127
Guerrini R., Carrozzo R., (2001). Epilepsy and genetic malformations of the cerebral cortex. Am. J. Med. Genet. Summer 106 160–173. 10.1002/ajmg.1569 11579436
Guerrini R., Marini C., Mantegazza M., (2014). Genetic epilepsy syndromes without structural brain abnormalities: clinical features and experimental models. Neurotherapeutics 11 269–285. 10.1007/s13311-014-0267-0 24664660
Guerrini R., Noebels J., (2014). How can advances in epilepsy genetics lead to better treatments and cures? Adv. Exp. Med. Biol. 813 309–317. 10.1007/978-94-017-8914-1_25 25012387
Hansen D. V., Lui J. H., Parker P. R., Kriegstein A. R., (2010). Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464 554–561. 10.1038/nature08845 20154730
Heide M., Long K. R., Huttner W. B., (2017). Novel gene function and regulation in neocortex expansion. Curr. Opin. Cell Biol. 49 22–30. 10.1016/j.ceb.2017.11.008 29227861
Ishii K., Kubo K. I., Nakajima K., (2016). Reelin and neuropsychiatric disorders. Front. Cell Neurosci. 10:229.
Janszky J., Ebner A., Kruse B., Mertens M., Jokeit H., Seitz R. J., (2003). Functional organization of the brain with malformations of cortical development. Ann. Neurol. 53 759–767. 12783422
Kalebic N., Gilardi C., Stepien B., Wilsch-Brauninger M., Long K. R., Namba T., (2019). Neocortical expansion due to increased proliferation of basal progenitors is linked to changes in their morphology. Cell Stem Cell 24:535-550.e9. 10.1016/j.stem.2019.02.017 30905618
Karzbrun E., Kshirsagar A., Cohen S. R., Hanna J. H., Reiner O., (2018). Human brain organoids on a chip reveal the physics of folding. Nat. Phys. 14 515–522. 10.1038/s41567-018-0046-7 29760764
Karzbrun E., Reiner O., (2019). Brain organoids-a bottom-up approach for studying human neurodevelopment. Bioengineering 6:E9. 10.3390/bioengineering6010009 30669275
Khacho M., Slack R. S., (2017). Mitochondrial activity in the regulation of stem cell self-renewal and differentiation. Curr. Opin. Cell Biol. 49 1–8. 10.1016/j.ceb.2017.11.003 29175320
Klaus J., Kanton S., Kyrousi C., Ayo-Martin A. C., Di Giaimo R., Riesenberg S., (2019). Altered neuronal migratory trajectories in human cerebral organoids derived from individuals with neuronal heterotopia. Nat. Med. 25 561–568. 10.1038/s41591-019-0371-0 30858616
Klonowski W., Korzynska A., Gomolka R., (2018). Computer analysis of histopathological images for tumor grading. Physiol. Meas. 39:034002. 10.1088/1361-6579/aaa82c 29337296
Klonowski W., Stepien R., Stepien P., (2010). Simple fractal method of assessment of histological images for application in medical diagnostics. Nonlinear Biomed. Phys. 4:7. 10.1186/1753-4631-4-7 21134258
Knezovic V., Kasprian G., Stajduhar A., Schwartz E., Weber M., Gruber G. M., (2019). Underdevelopment of the human hippocampus in callosal agenesis: an in vivo fetal MRI study. AJNR Am. J. Neuroradiol. 40 576–581. 10.3174/ajnr.A5986 30792247
Kostic M., Paridaen J., Long K. R., Kalebic N., Langen B., Grubling N., (2019). YAP activity is necessary and sufficient for basal progenitor abundance and proliferation in the developing neocortex. Cell Rep. 27:e1106. 10.1016/j.celrep.2019.03.091 31018127
Kyrousi C., Cappello S., (2019). Using brain organoids to study human neurodevelopment, evolution and disease. Wiley Interdiscip. Rev. Dev. Biol. 9:e347. 10.1002/wdev.347 31071759
Lancaster M. A., Renner M., Martin C. A., Wenzel D., Bicknell L. S., Hurles M. E., (2013). Cerebral organoids model human brain development and microcephaly. Nature 501 373–379. 10.1038/nature12517 23995685
Latham S. L., Ehmke N., Reinke P. Y. A., Taft M. H., Eicke D., Reindl T., (2018). Variants in exons 5 and 6 of ACTB cause syndromic thrombocytopenia. Nat. Commun. 9:4250. 10.1038/s41467-018-06713-0 30315159
Ledonne F., Orduz D., Mercier J., Vigier L., Grove E. A., Tissir F., (2016). Targeted inactivation of bax reveals a subtype-specific mechanism of cajal-retzius neuron death in the postnatal cerebral cortex. Cell Rep. 17 3133–3141. 10.1016/j.celrep.2016.11.074 28009284
Lee J. H., Huynh M., Silhavy J. L., Kim S., Dixon-Salazar T., Heiberg A., (2012). De novo somatic mutations in components of the PI3K-AKT3-mTOR pathway cause hemimegalencephaly. Nat. Genet. 44 941–945. 10.1038/ng.2329 22729223
Lim J. S., Kim W. I., Kang H. C., Kim S. H., Park A. H., Park E. K., (2015). Brain somatic mutations in MTOR cause focal cortical dysplasia type II leading to intractable epilepsy. Nat. Med. 21 395–400. 10.1038/nm.3824 25799227
Ljungberg M. C., Bhattacharjee M. B., Lu Y., Armstrong D. L., Yoshor D., Swann J. W., (2006). Activation of mammalian target of rapamycin in cytomegalic neurons of human cortical dysplasia. Ann. Neurol. 60 420–429. 10.1002/ana.20949 16912980
Long K. R., Newland B., Florio M., Kalebic N., Langen B., Kolterer A., (2018). Extracellular matrix components HAPLN1, lumican, and collagen i cause hyaluronic acid-dependent folding of the developing human neocortex. Neuron 99:702-719.e6. 10.1016/j.neuron.2018.07.013 30078576
Lukaszewicz A., Savatier P., Cortay V., Giroud P., Huissoud C., Berland M., (2005). G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex. Neuron 47 353–364. 10.1016/j.neuron.2005.06.032 16055060
Malinger G., Kidron D., Schreiber L., Ben-Sira L., Hoffmann C., Lev D., (2007). Prenatal diagnosis of malformations of cortical development by dedicated neurosonography. Ultrasound Obstet. Gynecol. 29 178–191. 10.1002/uog.3906 17219377
Mansour A. A., Goncalves J. T., Bloyd C. W., Li H., Fernandes S., Quang D., (2018). An in vivo model of functional and vascularized human brain organoids. Nat. Biotechnol. 36 432–441. 10.1038/nbt.4127 29658944
Marsan E., Baulac S., (2018). Review: mechanistic target of rapamycin (mTOR) pathway, focal cortical dysplasia and epilepsy. Neuropathol. Appl. Neurobiol. 44 6–17. 10.1111/nan.12463 29359340
Martin P. T., (2005). The dystroglycanopathies: the new disorders of O-linked glycosylation. Semin. Pediatr. Neurol. 12 152–158. 10.1016/j.spen.2005.10.003 16584074
Mayer S., Chen J., Velmeshev D., Mayer A., Eze U. C., Bhaduri A., (2019). Multimodal single-cell analysis reveals physiological maturation in the developing human neocortex. Neuron 102:e147. 10.1016/j.neuron.2019.01.027 30770253
Mei D., Parrini E., Marini C., Guerrini R., (2017). The impact of next-generation sequencing on the diagnosis and treatment of epilepsy in paediatric patients. Mol. Diagn. Ther. 21 357–373. 10.1007/s40291-017-0257-0 28197949
Meuwissen M. E., Schot R., Buta S., Oudesluijs G., Tinschert S., Speer S. D., (2016). Human USP18 deficiency underlies type 1 interferonopathy leading to severe pseudo-TORCH syndrome. J. Exp. Med. J. 213 1163–1174. 10.1084/jem.20151529 27325888
Miller D. J., Bhaduri A., Sestan N., Kriegstein A., (2019). Shared and derived features of cellular diversity in the human cerebral cortex. Curr. Opin. Neurobiol. 56 117–124. 10.1016/j.conb.2018.12.005 30677551
Mills J. D., Iyer A. M., van Scheppingen J., Bongaarts A., Anink J. J., Janssen B., (2017). Coding and small non-coding transcriptional landscape of tuberous sclerosis complex cortical tubers: implications for pathophysiology and treatment. Sci. Rep. 7:8089. 10.1038/s41598-017-06145-8 28808237
Mirzaa G. M., Campbell C. D., Solovieff N., Goold C., Jansen L. A., Menon S., (2016). Association of MTOR mutations with developmental brain disorders, including megalencephaly, focal cortical dysplasia, and pigmentary mosaicism. JAMA Neurol. 73 836–845. 10.1001/jamaneurol.2016.0363 27159400
Miyata H., Chiang A. C., Vinters H. V., (2004). Insulin signaling pathways in cortical dysplasia and TSC-tubers: tissue microarray analysis. Ann. Neurol. 56 510–519. 10.1002/ana.20234 15455398
Miyata T., Kawaguchi A., Okano H., Ogawa M., (2001). Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31 727–741. 10.1016/s0896-6273(01)00420-2 11567613
Mora-Bermudez F., Badsha F., Kanton S., Camp J. G., Vernot B., Kohler K., (2016). Differences and similarities between human and chimpanzee neural progenitors during cerebral cortex development. eLife 5:e18683. 10.7554/eLife.18683 27669147
Muhlebner A., Bongaarts A., Sarnat H. B., Scholl T., Aronica E., (2019). New insights into a spectrum of developmental malformations related to mTOR dysregulations: challenges and perspectives. J. Anat. 235 521–542. 10.1111/joa.12956 30901081
Nowakowski T. J., Bhaduri A., Pollen A. A., Alvarado B., Mostajo-Radji M. A., Di Lullo E., (2017). Spatiotemporal gene expression trajectories reveal developmental hierarchies of the human cortex. Science 358 1318–1323. 10.1126/science.aap8809 29217575
Oegema R., Baillat D., Schot R., van Unen L. M., Brooks A., Kia S. K., (2017). Human mutations in integrator complex subunits link transcriptome integrity to brain development. PLoS Genet. 13:e1006809. 10.1371/journal.pgen.1006809 28542170
Ohtaka-Maruyama C., Okamoto M., Endo K., Oshima M., Kaneko N., Yura K., (2018). Synaptic transmission from subplate neurons controls radial migration of neocortical neurons. Science 360 313–317. 10.1126/science.aar2866 29674592
Ostrem B., Di Lullo E., Kriegstein A., (2017). oRGs and mitotic somal translocation - a role in development and disease. Curr. Opin. Neurobiol. 42 61–67. 10.1016/j.conb.2016.11.007 27978479
Pacitti D., Privolizzi R., Bax B. E., (2019). Organs to cells and cells to organoids: the evolution of in vitro central nervous system modelling. Front. Cell Neurosci. 13:129. 10.3389/fncel.2019.00129 31024259
Paredes M. F., James D., Gil-Perotin S., Kim H., Cotter J. A., Ng C., (2016). Extensive migration of young neurons into the infant human frontal lobe. Science 354:aaf7073. 10.1126/science.aaf7073 27846470
Pham M. T., Pollock K. M., Rose M. D., Cary W. A., Stewart H. R., Zhou P., (2018). Generation of human vascularized brain organoids. Neuroreport 29 588–593. 10.1097/WNR.0000000000001014 29570159
Plantier V., Watrin F., Buhler E., Martineau F. S., Sahu S., Manent J. B., (2018). Direct and collateral alterations of functional cortical circuits in a rat model of subcortical band heterotopia. Cereb. Cortex 29 4253–4262. 10.1093/cercor/bhy307 30534979
Qian X., Jacob F., Song M. M., Nguyen H. N., Song H., Ming G. L., (2018). Generation of human brain region-specific organoids using a miniaturized spinning bioreactor. Nat. Protoc. 13 565–580. 10.1038/nprot.2017.152 29470464
Rainger J., Williamson K. A., Soares D. C., Truch J., Kurian D., Gillessen-Kaesbach G., (2017). A recurrent de novo mutation in ACTG1 causes isolated ocular coloboma. Hum. Mutat. 38 942–946. 10.1002/humu.23246 28493397
Reiner O., Carrozzo R., Shen Y., Wehnert M., Faustinella F., Dobyns W. B., (1993). Isolation of a Miller-Dieker lissencephaly gene containing G protein beta-subunit-like repeats. Nature 364 717–721. 10.1038/364717a0 8355785
Ribierre T., Deleuze C., Bacq A., Baldassari S., Marsan E., Chipaux M., (2018). Second-hit mosaic mutation in mTORC1 repressor DEPDC5 causes focal cortical dysplasia-associated epilepsy. J. Clin. Invest. 128 2452–2458. 10.1172/JCI99384 29708508
Rom A., Melamed L., Goldrich M. J., Kadir R., Golan M., Biton I., (2019). Regulation of CHD2 expression by the Chaserr long noncoding RNA is essential for viability. bioRxiv 536771.
Sahu S., Buhler E., Vermoyal J. C., Watrin F., Represa A., Manent J. B., (2019). Spontaneous epileptiform activity in a rat model of bilateral subcortical band heterotopia. Epilepsia 60 337–348. 10.1111/epi.14633 30597542
Sanai N., Nguyen T., Ihrie R. A., Mirzadeh Z., Tsai H. H., Wong M., (2011). Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478 382–386. 10.1038/nature10487 21964341
Schulze T. G., McMahon F. J., (2004). Defining the phenotype in human genetic studies: forward genetics and reverse phenotyping. Hum. Hered. 58 131–138. 10.1159/000083539 15812169
Sekine K., Honda T., Kawauchi T., Kubo K., Nakajima K., (2011). The outermost region of the developing cortical plate is crucial for both the switch of the radial migration mode and the Dab1-dependent “inside-out” lamination in the neocortex. J. Neurosci. 31 9426–9439. 10.1523/JNEUROSCI.0650-11.2011 21697392
Silva C. G., Peyre E., Adhikari M. H., Tielens S., Tanco S., Van Damme P., (2018). Cell-Intrinsic control of interneuron migration drives cortical morphogenesis. Cell 172:e1019. 10.1016/j.cell.2018.01.031 29474907
Skogseid I. M., Rosby O., Konglund A., Connelly J. P., Nedregaard B., Jablonski G. E., (2018). Dystonia-deafness syndrome caused by ACTB p.Arg183Trp heterozygosity shows striatal dopaminergic dysfunction and response to pallidal stimulation. J. Neurodev. Disord. 10:17. 10.1186/s11689-018-9235-z 29788902
Smart I. H., Dehay C., Giroud P., Berland M., Kennedy H., (2002). Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb. Cortex 12 37–53. 10.1093/cercor/12.1.37 11734531
Sun T., Hevner R. F., (2014). Growth and folding of the mammalian cerebral cortex: from molecules to malformations. Nat. Rev. Neurosci. 15 217–232. 10.1038/nrn3707 24646670
Tabata H., Nakajima K., (2003). Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J. Neurosci. 23 9996–10001. 10.1523/jneurosci.23-31-09996.2003 14602813
Vandervore L. V., Schot R., Kasteleijn E., Oegema R., Stouffs K., Gheldof A., (2019). Heterogeneous clinical phenotypes and cerebral malformations reflected by rotatin cellular dynamics. Brain 142 867–884. 10.1093/brain/awz045 30879067
Yates T. M., Turner C. L., Firth H. V., Berg J., Pilz D. T., (2017). Baraitser-Winter cerebrofrontofacial syndrome. Clin. Genet. 92 3–9. 10.1111/cge.12864 27625340