Cited by 243Neurogenesis and neuroplasticity mechanismsFetal and Pediatric Neurological DisordersGenetics and Neurodevelopmental Disorders

The DOI matches its Crossref record; 213 of the 216 references it cites were found in a registry or an index.

Deconstructing cortical folding: genetic, cellular and mechanical determinants

Llinares-Benadero, Cristina, Borrell, Víctor·2019·Nature Reviews Neuroscience

DOI 10.1038/s41583-018-0112-2

Open this paper in CoChat — free account

Abstract

Folding of the cerebral cortex is a fundamental milestone of mammalian brain evolution and is associated with dramatic increases in size and complexity. New animal models, genetic tools and bioengineering materials have moved the study of cortical folding from simple phenomenological observation to sophisticated experimental testing. Here, we provide an overview of how genetics, cell biology and biomechanics shape this complex and multifaceted process and affect each other. We discuss the evolution of cortical folding and the genomic changes in the primate lineage that seem to be responsible for the advent of larger brains and cortical folding. Emerging technologies now provide unprecedented tools to analyse and manipulate cortical folding, with the promise of elucidating the mechanisms underlying the stereotyped folding of the cerebral cortex in its full complexity.

Integrity signals

Registry

Crossref · 10.1038/s41583-018-0112-2

Cites

213 of 213 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Matrix elasticity directs stem cell lineage specification
Engler, A. J., Sen, S., Sweeney, H. L., & Discher, D. E. (2006) · Cell · doi:10.1016/j.cell.2006.06.044 · Cited by 13,915
Initial sequencing and comparative analysis of the mouse genome
Mouse Genome Sequencing Consortium (2002) · Nature · doi:10.1038/nature01262 · Cited by 7,187
Cell Shape, Cytoskeletal Tension, and RhoA Regulate Stem Cell Lineage Commitment
McBeath, R., Pirone, D. M., Nelson, C. M., Bhadriraju, K., & Chen, C. S. (2004) · Developmental Cell · doi:10.1016/s1534-5807(04)00075-9 · Cited by 4,182
Evolution at Two Levels in Humans and Chimpanzees: Their macromolecules are so alike that regulatory mutations may account for their biological differences
King, M.-C., & Wilson, A. C. (1975) · Science · doi:10.1126/science.1090005 · Cited by 2,815
Cellular Scaling Rules for the Brains of Marsupials: Not as “Primitive” as Expected
Santos, S. E. D., Porfírio, J., Cunha, F., Manger, P. R., Tavares, W. C., Pessôa, L. M., Raghanti, M. A., Sherwood, C. C., & Herculano‐Houzel, S. (2017) · Brain Behavior and Evolution · doi:10.1159/000452856 · Cited by 2,652
Mode of cell migration to the superficial layers of fetal monkey neocortex
Rakic, P. (1972) · Journal of Comparative Neurology · doi:10.1002/cne.901450105 · Cited by 2,170
The delayed rise of present-day mammals
Bininda-Emonds, O. R. P., Cardillo, M., Jones, K. E., MacPhee, R. D. E., Beck, R. M. D., Grenyer, R., Price, S. A., Vos, R. A., Gittleman, J. L., & Purvis, A. (2007) · Nature · doi:10.1038/nature05634 · Cited by 2,082
A protein related to extracellular matrix proteins deleted in the mouse mutant reeler
D'Arcangelo, G., G. Miao, G., Chen, S.-C., Scares, H. D., Morgan, J. I., & Curran, T. (1995) · Nature · doi:10.1038/374719a0 · Cited by 1,748
A tension-based theory of morphogenesis and compact wiring in the central nervous system
Essen, D. C. V. (1997) · Nature · doi:10.1038/385313a0 · Cited by 1,668
Regulation of Cerebral Cortical Size by Control of Cell Cycle Exit in Neural Precursors
Chenn, A., & Walsh, C. A. (2002) · Science · doi:10.1126/science.1074192 · Cited by 1,431
Neurogenic radial glia in the outer subventricular zone of human neocortex
Hansen, D. V., Lui, J. H., Parker, P. R. L., & Kriegstein, A. R. (2010) · Nature · doi:10.1038/nature08845 · Cited by 1,388
Doublecortin Is a Microtubule-Associated Protein and Is Expressed Widely by Migrating Neurons
Gleeson, J. G., Lin, P. T., Flanagan, L. A., & Walsh, C. A. (1999) · Neuron · doi:10.1016/s0896-6273(00)80778-3 · Cited by 1,365
Development and Evolution of the Human Neocortex
Lui, J. H., Hansen, D. V., & Kriegstein, A. R. (2011) · Cell · doi:10.1016/j.cell.2011.06.030 · Cited by 1,342
Transcriptional landscape of the prenatal human brain
Miller, J. A., Ding, S.-L., Sunkin, S. M., Smith, K. A., Ng, L., Szafer, A., Ebbert, A., Riley, Z. L., Royall, J. J., Aiona, K., et al. (2014) · Nature · doi:10.1038/nature13185 · Cited by 1,325
Neuronal migration, with special reference to developing human brain: a review
Sidman, R. L., & RAKIC, P. T. (1973) · Brain Research · doi:10.1016/0006-8993(73)90617-3 · Cited by 1,260
The Placental Mammal Ancestor and the Post–K-Pg Radiation of Placentals
O’Leary, M. A., Bloch, J. I., Flynn, J. J., Gaudin, T. J., Giallombardo, A., Giannini, N. P., Goldberg, S. L., Kraatz, B., Luo, Z., Meng, J., et al. (2013) · Science · doi:10.1126/science.1229237 · Cited by 1,222
A developmental and genetic classification for malformations of cortical development: update 2012
Barkovich, A. J., Guerrini, R., Kuzniecky, R., Jackson, G. D., & Dobyns, W. B. (2012) · Brain · doi:10.1093/brain/aws019 · Cited by 1,146
Doublecortin Is a Developmentally Regulated, Microtubule-Associated Protein Expressed in Migrating and Differentiating Neurons
Francis, F., Koulakoff, A., Boucher, D., Chafey, P., Schaar, B. T., Vinet, M. C., Friocourt, G., McDonnell, N., Reiner, O., Kahn, A., et al. (1999) · Neuron · doi:10.1016/s0896-6273(00)80777-1 · Cited by 1,014
An RNA gene expressed during cortical development evolved rapidly in humans
Pollard, K. S., Salama, S. R., Lambert, N., Lambot, M.-A., Coppens, S., Pedersen, J. S., Katzman, S., King, B., Onodera, C., Siepel, A., et al. (2006) · Nature · doi:10.1038/nature05113 · Cited by 1,005
Spatiotemporal gene expression trajectories reveal developmental hierarchies of the human cortex
Nowakowski, T. J., Bhaduri, A., Pollen, A. A., Alvarado, B., Mostajo-Radji, M. A., Di Lullo, E., Haeussler, M., Sandoval-Espinosa, C., Liu, S. J., Velmeshev, D., et al. (2017) · Science · doi:10.1126/science.aap8809 · Cited by 964
Low-coverage single-cell mRNA sequencing reveals cellular heterogeneity and activated signaling pathways in developing cerebral cortex
Pollen, A. A., Nowakowski, T. J., Shuga, J., Wang, X., Leyrat, A. A., Lui, J. H., Li, N., Szpankowski, L., Fowler, B., Chen, P., et al. (2014) · Nature Biotechnology · doi:10.1038/nbt.2967 · Cited by 920
Molecular Identity of Human Outer Radial Glia during Cortical Development
Pollen, A. A., Nowakowski, T. J., Chen, J., Retallack, H., Sandoval-Espinosa, C., Nicholas, C. R., Shuga, J., Liu, S. J., Oldham, M. C., Diaz, A., et al. (2015) · Cell · doi:10.1016/j.cell.2015.09.004 · Cited by 908
Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations
Hong, S. E., Shugart, Y. Y., Huang, D. T.-C., Shahwan, S. A., Grant, P. E., Hourihane, J. O., Martin, N. D. T., & Walsh, C. A. (2000) · Nature Genetics · doi:10.1038/79246 · Cited by 896
OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling
Fietz, S. A., Kelava, I., Vogt, J., Wilsch-Bräuninger, M., Stenzel, D., Fish, J. L., Corbeil, D., Riehn, A., Distler, W., Nitsch, R., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2553 · Cited by 830
De novo germline and postzygotic mutations in AKT3, PIK3R2 and PIK3CA cause a spectrum of related megalencephaly syndromes
Finding of Rare Disease Genes (FORGE) Canada Consortium, Rivière, J.-B., Mirzaa, G. M., O'Roak, B. J., Beddaoui, M., Alcantara, D., Conway, R. L., St-Onge, J., Schwartzentruber, J. A., Gripp, K. W., et al. (2012) · Nature Genetics · doi:10.1038/ng.2331 · Cited by 741
Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion
Kriegstein, A., Noctor, S., & Martínez-Cerdeño, V. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn2008 · Cited by 738
Mutation of ARX causes abnormal development of forebrain and testes in mice and X-linked lissencephaly with abnormal genitalia in humans
Kitamura, K., Yanazawa, M., Sugiyama, N., Miura, H., Iizuka‐Kogo, A., Kusaka, M., Omichi, K., Suzuki, R., Fukui, Y., Kamiirisa, K., et al. (2002) · Nature Genetics · doi:10.1038/ng1009 · Cited by 726
De novo somatic mutations in components of the PI3K-AKT3-mTOR pathway cause hemimegalencephaly
Lee, J. H., Huynh, M., Silhavy, J. L., Kim, S., Dixon-Salazar, T., Heiberg, A., Scott, E., Bafna, V., Hill, K. J., Collazo, A., et al. (2012) · Nature Genetics · doi:10.1038/ng.2329 · Cited by 703
A single-cell RNA-seq survey of the developmental landscape of the human prefrontal cortex
Zhong, S., Zhang, S., Fan, X., Wu, Q., Yan, L., Dong, J., Zhang, H., Li, L., Sun, L., Pan, N., et al. (2018) · Nature · doi:10.1038/nature25980 · Cited by 689
Unique Morphological Features of the Proliferative Zones and Postmitotic Compartments of the Neural Epithelium Giving Rise to Striate and Extrastriate Cortex in the Monkey
Smart, I. H. M. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.1.37 · Cited by 687
Role of the Reelin Signaling Pathway in Central Nervous System Development
Rice, D. S., & Curran, T. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1005 · Cited by 667
Cell-cycle control and cortical development
Dehay, C., & Kennedy, H. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2097 · Cited by 655
A Role for Intermediate Radial Glia in the Tangential Expansion of the Mammalian Cerebral Cortex
Reillo, I., Romero, C. D. J., García‐Cabezas, M. Á., & Borrell, V. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq238 · Cited by 655
Self-citation
Human-specific gene ARHGAP11B promotes basal progenitor amplification and neocortex expansion
Florio, M., Albert, M., Taverna, E., Namba, T., Brandl, H., Lewitus, E., Haffner, C., Sykes, A., Wong, F. K., Peters, J., et al. (2015) · Science · doi:10.1126/science.aaa1975 · Cited by 632
Human-Specific NOTCH2NL Genes Affect Notch Signaling and Cortical Neurogenesis
Fiddes, I. T., Lodewijk, G. A., Mooring, M., Bosworth, C. M., Ewing, A. D., Mantalas, G. L., Novak, A. M., van den Bout, A., Bishara, A., Rosenkrantz, J. L., et al. (2018) · Cell · doi:10.1016/j.cell.2018.03.051 · Cited by 595
Calcium Waves Propagate through Radial Glial Cells and Modulate Proliferation in the Developing Neocortex
Weissman, T. A., Riquelme, P. A., Ivic, L., Flint, A. C., & Kriegstein, A. R. (2004) · Neuron · doi:10.1016/j.neuron.2004.08.015 · Cited by 586
On the growth and form of cortical convolutions
Tallinen, T., Chung, J. Y., Rousseau, F., Girard, N. J., Lefèvre, J., & Mahadevan, L. (2016) · Nature Physics · doi:10.1038/nphys3632 · Cited by 581
Viscoelastic properties of individual glial cells and neurons in the CNS
Lu, Y., Franze, K., Seifert, G., Steinhäuser, C., Kirchhoff, F., Wolburg, H., Guck, J. R., Janmey, P. A., Wei, E.-Q., Käs, J. A., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0606150103 · Cited by 580
Reelin Binds α3β1 Integrin and Inhibits Neuronal Migration
Dulabon, L., Olson, E. C., Taglienti, M. G., Eisenhuth, S., McGrath, B., Walsh, C. A., Kreidberg, J. A., & Anton, E. S. (2000) · Neuron · doi:10.1016/s0896-6273(00)00007-6 · Cited by 577
Mechanical Model of Brain Convolutional Development
Richman, D. P., Stewart, R. M., Hutchinson, J. W., & Caviness, V. S. (1975) · Science · doi:10.1126/science.1135626 · Cited by 575
Development of cortical folding during evolution and ontogeny
Zilles, K., Palomero‐Gallagher, N., & Amunts, K. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.01.006 · Cited by 567
Development of glial cells in the cerebral wall of ferrets: Direct tracing of their transformation from radial glia into astrocytes
Voigt, T. B. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902890106 · Cited by 549
Mechanical Induction of Twist in the Drosophila Foregut/Stomodeal Primordium
Farge, E. (2003) · Current Biology · doi:10.1016/s0960-9822(03)00576-1 · Cited by 513
Forces shaping the fastest evolving regions in the human genome
Pollard, K. S., Salama, S. R., King, B., Kern, A. D., Dreszer, T., Katzman, S., Siepel, A., Pedersen, J. S., Bejerano, G., Baertsch, R., et al. (2006) · PLoS Genetics · doi:10.1371/journal.pgen.0020168 · Cited by 511
A distal enhancer and an ultraconserved exon are derived from a novel retroposon
Bejerano, G., Lowe, C. B., Ahituv, N., King, B., Siepel, A. C., Salama, S. R., Rubin, E. M., Kent, W. J., & Haussler, D. H. (2006) · Nature · doi:10.1038/nature04696 · Cited by 508
A new subtype of progenitor cell in the mouse embryonic neocortex
Wang, X., Tsai, J.-W., LaMonica, B., & Kriegstein, A. R. (2011) · Nature Neuroscience · doi:10.1038/nn.2807 · Cited by 507
Microcephalin , a Gene Regulating Brain Size, Continues to Evolve Adaptively in Humans
Evans, P. D., Gilbert, S. L., Mekel-Bobrov, N., Vallender, E. J., Anderson, J. R., Vaezazizi, L. M., Tishkoff, S. A., Hudson, R. R., & Lahn, B. T. (2005) · Science · doi:10.1126/science.1113722 · Cited by 506
Growth and folding of the mammalian cerebral cortex: from molecules to malformations
Sun, T., & Hevner, R. F. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3707 · Cited by 489
Mutations in TUBG1, DYNC1H1, KIF5C and KIF2A cause malformations of cortical development and microcephaly
Poirier, K., Lebrun, N., Broix, L., Tian, G., Saillour, Y., Boscheron, C., Parrini, E., Valence, S., Saintpierre, B., Oger, M., et al. (2013) · Nature Genetics · doi:10.1038/ng.2613 · Cited by 479
Oblique Radial Glial Divisions in the Developing Mouse Neocortex Induce Self-Renewing Progenitors outside the Germinal Zone That Resemble Primate Outer Subventricular Zone Progenitors
Shitamukai, A., Konno, D., & Matsuzaki, F. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4773-10.2011 · Cited by 474
Human-Specific NOTCH2NL Genes Expand Cortical Neurogenesis through Delta/Notch Regulation
Suzuki, I. K., Gacquer, D., Van Heurck, R., Kumar, D., Wojno, M., Bilheu, A., Herpoel, A., Lambert, N., Cheron, J., Polleux, F., et al. (2018) · Cell · doi:10.1016/j.cell.2018.03.067 · Cited by 471
Mapping the Early Cortical Folding Process in the Preterm Newborn Brain
Dubois, J., Benders, M. J. N. L., Cachia, A., Lazeyras, F., Leuchter, R. H., Sizonenko, S. V., Borradori-Tolsa, C., Mangin, J., & Hüppi, P. S. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm180 · Cited by 468
Ongoing Adaptive Evolution of ASPM , a Brain Size Determinant in Homo sapiens
Mekel-Bobrov, N., Gilbert, S. L., Evans, P. D., Vallender, E. J., Anderson, J. R., Hudson, R. R., Tishkoff, S. A., & Lahn, B. T. (2005) · Science · doi:10.1126/science.1116815 · Cited by 463
Precursor Diversity and Complexity of Lineage Relationships in the Outer Subventricular Zone of the Primate
Betizeau, M., Cortay, V., Patti, D., Pfister, S., Gautier, E., Bellemin-Ménard, A., Afanassieff, M., Huissoud, C., Douglas, R. J., Kennedy, H., et al. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.032 · Cited by 462
Induction of Expansion and Folding in Human Cerebral Organoids
Li, Y., Muffat, J., Omer, A., Bosch, I., Lancaster, M. A., Sur, M., Gehrke, L., Knoblich, J. A., & Jaenisch, R. (2017) · Cell Stem Cell · doi:10.1016/j.stem.2016.11.017 · Cited by 436
Why Does Cerebral Cortex Fissure and Fold?
Welker, W. I. (1990) · Cerebral cortex · doi:10.1007/978-1-4615-3824-0_1 · Cited by 433
Accelerated Evolution of Nervous System Genes in the Origin of Homo sapiens
Dorus, S., Vallender, E. J., Evans, P. D., Anderson, J. R., Gilbert, S. L., Mahowald, M. A., Wyckoff, G. J., Malcom, C. M., & Lahn, B. T. (2004) · Cell · doi:10.1016/j.cell.2004.11.040 · Cited by 429
Human brain organoids on a chip reveal the physics of folding
Karzbrun, E., Kshirsagar, A., Cohen, S., Hanna, J. H., & Reiner, O. (2018) · Nature Physics · doi:10.1038/s41567-018-0046-7 · Cited by 421
Gyrification from constrained cortical expansion
Tallinen, T., Chung, J. Y., Biggins, J. S., & Mahadevan, L. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1406015111 · Cited by 418
Retinoic acid from the meninges regulates cortical neuron generation.
Siegenthaler, J. A., Ashique, A. M., Zarbalis, K., Patterson, K. P., Hecht, J. H., Kane, M. A., Folias, A. E., Choe, Y., May, S. R., Kume, T., et al. (2009) · Cell · doi:10.1016/j.cell.2009.10.004 · Cited by 402
Axonal growth in response to experimentally applied mechanical tension
Bray, D. (1984) · Developmental Biology · doi:10.1016/0012-1606(84)90202-1 · Cited by 391
Cerebral cortex expansion and folding: what have we learned?
Fernández, V., Llinares-Benadero, C., & Borrell, V. (2016) · The EMBO Journal · doi:10.15252/embj.201593701 · Cited by 382
Self-citation
Transformation of the Radial Glia Scaffold Demarcates Two Stages of Human Cerebral Cortex Development
Nowakowski, T. J., Pollen, A. A., Sandoval-Espinosa, C., & Kriegstein, A. R. (2016) · Neuron · doi:10.1016/j.neuron.2016.09.005 · Cited by 362
LIS1 and XLIS (DCX) mutations cause most classical lissencephaly, but different patterns of malformation
Pilz, D. T. (1998) · Human Molecular Genetics · doi:10.1093/hmg/7.13.2029 · Cited by 360
Human-Specific Gain of Function in a Developmental Enhancer
Prabhakar, S., Visel, A., Akiyama, J. A., Shoukry, M. I., Lewis, K. D., Holt, A., Plajzer-Frick, I., Morrison, H., FitzPatrick, D. R., Afzal, V., et al. (2008) · Science · doi:10.1126/science.1159974 · Cited by 357
A Morphogenetic Model for the Development of Cortical Convolutions
Toro, R., & Burnod, Y. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhi068 · Cited by 339
Physical biology of human brain development
Budday, S., Steinmann, P., & Ellen Kuhl, A. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00257 · Cited by 337
Transcriptomes of germinal zones of human and mouse fetal neocortex suggest a role of extracellular matrix in progenitor self-renewal
Fietz, S. A., Lachmann, R., Brandl, H., Kircher, M., Samusik, N., Schröder, R., Lakshmanaperumal, N., Henry, I., Vogt, J., Riehn, A., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1209647109 · Cited by 337
Transgenic Monkeys Produced by Retroviral Gene Transfer into Mature Oocytes
Chan, A. W. S., Chong, K., Martinovich, C., Simerly, C. R., & Schatten, G. P. (2001) · Science · doi:10.1126/science.291.5502.309 · Cited by 315
G1 Phase Regulation, Area-Specific Cell Cycle Control, and Cytoarchitectonics in the Primate Cortex
Lukaszewicz, A., Savatier, P., Cortay, V., Giroud, P., Huissoud, C., Berland, M., Kennedy, H., & Dehay, C. (2005) · Neuron · doi:10.1016/j.neuron.2005.06.032 · Cited by 315
The outer subventricular zone and primate-specific cortical complexification
Dehay, C., Kennedy, H., & Kosik, K. S. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.060 · Cited by 314
Role of Mechanical Factors in the Morphology of the Primate Cerebral Cortex
Hilgetag, C. C., & Barbas, H. (2005) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0020022 · Cited by 311
Further Delineation of Deletion 1p36 Syndrome in 60 Patients: A Recognizable Phenotype and Common Cause of Developmental Delay and Mental Retardation
Battaglia, A., Hoyme, H. E., Dallapiccola, B., Zackai, E. H., Hudgins, L., McDonald‐McGinn, D. M., Bahi‐Buisson, N., Romano, C., Williams, C. A., Brailey, L. L., et al. (2008) · PEDIATRICS · doi:10.1542/peds.2007-0929 · Cited by 308
Reduction of microtubule catastrophe events by LIS1, platelet‐activating factor acetylhydrolase subunit
Sapir, T., Elbaum, M., & Reiner, O. (1997) · The EMBO Journal · doi:10.1093/emboj/16.23.6977 · Cited by 304
Gene Duplication: The Genomic Trade in Spare Parts
Hurles, M. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020206 · Cited by 298
Mutations in WDR62, encoding a centrosome-associated protein, cause microcephaly with simplified gyri and abnormal cortical architecture
Yu, T. W., Mochida, G. H., Tischfield, D. J., Sgaier, S. K., Flores‐Sarnat, L., Sergi, C. M., Topçu, M., McDonald, M., Barry, B. J., Felie, J. M., et al. (2010) · Nature Genetics · doi:10.1038/ng.683 · Cited by 294
Morphogenesis of Growing Soft Tissues
Dervaux, J., & Amar, M. B. (2008) · Physical Review Letters · doi:10.1103/physrevlett.101.068101 · Cited by 289
Single-cell analysis reveals transcriptional heterogeneity of neural progenitors in human cortex
Johnson, M. B., Wang, P. P., Atabay, K. D., Murphy, E. A., Doan, R. N., Hecht, J. L., & Walsh, C. A. (2015) · Nature Neuroscience · doi:10.1038/nn.3980 · Cited by 288
Cortical folding scales universally with surface area and thickness, not number of neurons
Mota, B., & Herculano‐Houzel, S. (2015) · Science · doi:10.1126/science.aaa9101 · Cited by 286
Ephrin signalling controls brain size by regulating apoptosis of neural progenitors
Depaepe, V., Gonzalez, N. S., Dufour, A., Passante, L., Gorski, J. A., Jones, K. R., Ledent, C. A., & Vanderhaeghen, P. (2005) · Nature · doi:10.1038/nature03651 · Cited by 284
Axons Pull on the Brain, But Tension Does Not Drive Cortical Folding
Xu, G., Knutsen, A. K., Dikranian, K. T., Kroenke, C. D., Bayly, P. V., & Taber, L. A. (2010) · Journal of Biomechanical Engineering · doi:10.1115/1.4001683 · Cited by 280
SRPX2 mutations in disorders of language cortex and cognition
Roll, P., Rudolf, G., Pereira, S., Royer, B., Scheffer, I. E., Massacrier, A., Valenti, M., Roëckel, N., Jamali, S., Béclin, C., et al. (2006) · Human Molecular Genetics · doi:10.1093/hmg/ddl035 · Cited by 277
Neuroepithelial Stem Cell Proliferation Requires LIS1 for Precise Spindle Orientation and Symmetric Division
Yingling, J., Youn, Y. H., Darling, D. L., Toyo‐oka, K., Pramparo, T., Hirotsune, S., & Wynshaw-Boris, A. J. (2008) · Cell · doi:10.1016/j.cell.2008.01.026 · Cited by 271
Trnp1 Regulates Expansion and Folding of the Mammalian Cerebral Cortex by Control of Radial Glial Fate
Stahl, R., Walcher, T., Romero, C. D. J., Pilz, G.-A., Cappello, S., Irmler, M., Sanz-Aquela, J. M., Beckers, J., Blum, R., Borrell, V., et al. (2013) · Cell · doi:10.1016/j.cell.2013.03.027 · Cited by 267
Self-citation
The cytomechanics of axonal elongation and retraction.
Dennerll, T. J., Lamoureux, P., Buxbaum, R. E., & Heidemann, S. R. (1989) · The Journal of Cell Biology · doi:10.1083/jcb.109.6.3073 · Cited by 264
The BRAIN Initiative Cell Census Consortium: Lessons Learned toward Generating a Comprehensive Brain Cell Atlas
Ecker, J. R., Geschwind, D. H., Kriegstein, A. R., Ngai, J., Osten, P., Polioudakis, D., Regev, A., Šestan, N., Wickersham, I. R., & Zeng, H. (2017) · Neuron · doi:10.1016/j.neuron.2017.10.007 · Cited by 258
Embryonic brain enlargement requires cerebrospinal fluid pressure
Desmond, M. E., & Jacobson, A. G. (1977) · Developmental Biology · doi:10.1016/0012-1606(77)90364-5 · Cited by 257
Non-proliferative effects of lysophosphatidic acid enhance cortical growth and folding
Kingsbury, M. A., Rehen, S. K., Contos, J. J. A., Higgins, C., & Chun, J. J. M. (2003) · Nature Neuroscience · doi:10.1038/nn1157 · Cited by 251
The role of mechanics during brain development
Budday, S., Steinmann, P., & Ellen Kuhl, A. (2014) · Journal of the Mechanics and Physics of Solids · doi:10.1016/j.jmps.2014.07.010 · Cited by 246
Mitotic spindle orientation predicts outer radial glial cell generation in human neocortex
Ostrem, B. E. L., Lui, J. H., Hansen, D. V., & Kriegstein, A. R. (2013) · Nature Communications · doi:10.1038/ncomms2647 · Cited by 244
The Role of Cell Death in Regulating the Size and Shape of the Mammalian Forebrain
Haydar, T. F. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.6.621 · Cited by 242
Adaptive evolution of ASPM, a major determinant of cerebral cortical size in humans
Evans, P. D., Anderson, J. R., Vallender, E. J., Gilbert, S. L., Malcom, C. M., Dorus, S., & Lahn, B. T. (2004) · Human Molecular Genetics · doi:10.1093/hmg/ddh055 · Cited by 240
Many human accelerated regions are developmental enhancers
Capra, J. A., Erwin, G. D., McKinsey, G., Rubenstein, J. L. R., & Pollard, K. S. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0025 · Cited by 235
Human Brain Malformations and Their Lessons for Neuronal Migration
Ross, M. E., & Walsh, C. A. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1041 · Cited by 235
Role of radial glial cells in cerebral cortex folding
Borrell, V., & Götz, M. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.02.007 · Cited by 230
Self-citation
Roles of the cytoskeleton, cell adhesion and rho signalling in mechanosensing and mechanotransduction
Ohashi, K., Fujiwara, S., & Mizuno, K. (2017) · The Journal of Biochemistry · doi:10.1093/jb/mvw082 · Cited by 230
Evolutionarily Dynamic Alternative Splicing of GPR56 Regulates Regional Cerebral Cortical Patterning
Bae, B.-I., Tietjen, I., Atabay, K. D., Evrony, G. D., Johnson, M. B., Asare, E., Wang, P. P., Murayama, A. Y., Im, K., Lisgo, S. N., et al. (2014) · Science · doi:10.1126/science.1244392 · Cited by 229
Amplification of progenitors in the mammalian telencephalon includes a new radial glial cell type
Pilz, G.-A., Shitamukai, A., Reillo, I., Pacary, E., Schwausch, J., Stahl, R., Ninkovic, J., Snippert, H. J. G., Clevers, H. C., Godinho, L., et al. (2013) · Nature Communications · doi:10.1038/ncomms3125 · Cited by 229
Self-citation
Common marmoset as a new model animal for neuroscience research and genome editing technology
Kishi, N., Sato, K., Sasaki, E., & Okano, H. (2014) · Development Growth & Differentiation · doi:10.1111/dgd.12109 · Cited by 224
Regulation of cerebral cortex size and folding by expansion of basal progenitors
Nonaka‐Kinoshita, M., Reillo, I., Artegiani, B., Ángeles Martínez‐Martínez, M., Nelson, M., Borrell, V., & Calegari, F. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.96 · Cited by 221
Self-citation
Abundant Occurrence of Basal Radial Glia in the Subventricular Zone of Embryonic Neocortex of a Lissencephalic Primate, the Common Marmoset Callithrix jacchus
Kelava, I., Reillo, I., Murayama, A. Y., Kalinka, A. T., Stenzel, D., Tomančák, P., Matsuzaki, F., Lebrand, C., Sasaki, E., Schwamborn, J. C., et al. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr301 · Cited by 217
Self-citation
Genetic Basis of Brain Malformations
Parrini, E., Conti, V., Dobyns, W. B., & Guerrini, R. (2016) · Molecular Syndromology · doi:10.1159/000448639 · Cited by 210
TUBA1A mutations cause wide spectrum lissencephaly (smooth brain) and suggest that multiple neuronal migration pathways converge on alpha tubulins
Kumar, R. A., Pilz, D. T., Babatz, T. D., Cushion, T. D., Harvey, K., Topf, M., Yates, L. M., Robb, S. A., Uyanık, G., Mancini, G. M. S., et al. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq182 · Cited by 208
Comparative Analysis of the Subventricular Zone in Rat, Ferret and Macaque: Evidence for an Outer Subventricular Zone in Rodents
Martínez-Cerdeño, V., Cunningham, C. L., Camacho, J., Antczak, J. L., Prakash, A. N., Cziep, M. E., Walker, A. I., & Noctor, S. C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030178 · Cited by 203
Evolution and cell-type specificity of human-specific genes preferentially expressed in progenitors of fetal neocortex
Florio, M., Heide, M., Pinson, A., Brandl, H., Albert, M., Winkler, S., Wimberger, P., Huttner, W. Β., & Hiller, M. (2018) · eLife · doi:10.7554/elife.32332 · Cited by 201
Homozygous silencing of T-box transcription factor EOMES leads to microcephaly with polymicrogyria and corpus callosum agenesis
Baala, L., Briault, S., Etchevers, H., Laumonnier, F., Natiq, A., Amiel, J., Boddaert, N., Pïcard, C., Sbiti, A., Asermouh, A., et al. (2007) · Nature Genetics · doi:10.1038/ng1993 · Cited by 200
Hedgehog signaling promotes basal progenitor expansion and the growth and folding of the neocortex
Wang, L., Hou, S., & Han, Y.-G. (2016) · Nature Neuroscience · doi:10.1038/nn.4307 · Cited by 196
Extracellular matrix components HAPLN1, Lumican and collagen I cause hyaluronic acid-dependent folding of the developing human neocortex
Long, K. R., Newland, B., Florio, M., Kalebic, N., Langen, B., Kolterer, A., Wimberger, P., & Huttner, W. B. (2018) · Neuron · doi:10.1016/j.neuron.2018.07.013 · Cited by 196
Evolution of Cortical Neurogenesis in Amniotes Controlled by Robo Signaling Levels
Cárdenas, A., Villalba, A., Romero, C. D. J., Picó, E., Kyrousi, C., Tzika, A. C., Tessier‐Lavigne, M., Ma, L., Drukker, M., Cappello, S., et al. (2018) · Cell · doi:10.1016/j.cell.2018.06.007 · Cited by 190
Self-citation
Cadherin Adhesion, Tissue Tension, and Noncanonical Wnt Signaling Regulate Fibronectin Matrix Organization
Dzamba, B. J., Jakab, K., Marsden, M., Schwartz, M. A., & DeSimone, D. W. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.01.008 · Cited by 186
Emerging roles of neural stem cells in cerebral cortex development and evolution
Borrell, V., & Reillo, I. (2012) · Developmental Neurobiology · doi:10.1002/dneu.22013 · Cited by 185
Self-citation
Deep Sulcal Landmarks Provide an Organizing Framework for Human Cortical Folding
Lohmann, G., von Cramon, D. Y., & Colchester, A. C. F. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm174 · Cited by 185
Germinal Zones in the Developing Cerebral Cortex of Ferret: Ontogeny, Cell Cycle Kinetics, and Diversity of Progenitors
Reillo, I., & Borrell, V. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr284 · Cited by 184
Self-citation
A cortical folding model incorporating stress-dependent growth explains gyral wavelengths and stress patterns in the developing brain
Bayly, P. V., Okamoto, R. J., Xu, G., Shi, Y., & Taber, L. A. (2013) · Physical Biology · doi:10.1088/1478-3975/10/1/016005 · Cited by 179
Mouse Inscuteable Induces Apical-Basal Spindle Orientation to Facilitate Intermediate Progenitor Generation in the Developing Neocortex
Postiglione, M. P., Jüschke, C., Xie, Y., Haas, G. A., Charalambous, C., & Knoblich, J. A. (2011) · Neuron · doi:10.1016/j.neuron.2011.09.022 · Cited by 178
Genome-Wide Identification of Human Functional DNA Using a Neutral Indel Model
Lunter, G. A., Ponting, C. P., & Hein, J. (2006) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0020005 · Cited by 177
Mechanical tension contributes to clustering of neurotransmitter vesicles at presynaptic terminals
Siechen, S., Yang, S., Chiba, A., & Saif, M. T. A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0901867106 · Cited by 176
Discrete domains of gene expression in germinal layers distinguish the development of gyrencephaly
Romero, C. D. J., Bruder, C. E. G., Tomasello, U., Sanz‐Anquela, J. M., & Borrell, V. (2015) · The EMBO Journal · doi:10.15252/embj.201591176 · Cited by 175
Self-citation
The hominoid-specific gene TBC1D3 promotes generation of basal neural progenitors and induces cortical folding in mice
Ju, X.-C., Hou, Q.-Q., Sheng, A.-L., Wu, K.-Y., Zhou, Y., Jin, Y., Wen, T., Yang, Z., Wang, X., & Luo, Z. (2016) · eLife · doi:10.7554/elife.18197 · Cited by 175
The Alignment of Migrating Neural Cells in Relation to the Murine Neopallial Radial Glial Fiber System
Mission, J., Austin, C. P., Takahashi, T., et al. (1991) · Cerebral Cortex · doi:10.1093/cercor/1.3.221 · Cited by 174
Aspm knockout ferret reveals an evolutionary mechanism governing cerebral cortical size
Johnson, M. B., Sun, X., Kodani, A., Borges-Monroy, R., Girskis, K. M., Ryu, S. C., Wang, P. P., Patel, K., Gonzalez, D. M., Woo, Y. M., et al. (2018) · Nature · doi:10.1038/s41586-018-0035-0 · Cited by 172
An Adaptive Threshold in Mammalian Neocortical Evolution
Lewitus, É., Kelava, I., Kalinka, A. T., Tomančák, P., & Huttner, W. Β. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1002000 · Cited by 169
Slit/Robo Signaling Modulates the Proliferation of Central Nervous System Progenitors
Borrell, V., Cárdenas, A., Ciceri, G., Galcerán, J., Flames, N., Pla, R., Pereira, S. N., Garcı́a-Frigola, C., Peregrín, S., Zhao, Z., et al. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.003 · Cited by 167
Self-citation
Mechanics of cortical folding: stress, growth and stability
Garcia, K., Kroenke, C. D., & Bayly, P. V. (2018) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2017.0321 · Cited by 165
FLRT2 and FLRT3 act as repulsive guidance cues for Unc5‐positive neurons
Yamagishi, S., Hampel, F., Hata, K., del Toro, D., Schwark, M., Kvachnina, E., Bastmeyer, M., Yamashita, T., Tarabykin, V. S., Klein, R., et al. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.189 · Cited by 162
Sodium Channel SCN3A (NaV1.3) Regulation of Human Cerebral Cortical Folding and Oral Motor Development
Smith, R. S., Kenny, C. J., Ganesh, V., Jang, A., Borges-Monroy, R., Partlow, J. N., Hill, R. S., Shin, T., Chen, A. Y., Doan, R. N., et al. (2018) · Neuron · doi:10.1016/j.neuron.2018.07.052 · Cited by 160
The evolution and population diversity of human-specific segmental duplications
Dennis, M. Y., Harshman, L., Nelson, B. J., Penn, O., Cantsilieris, S., Huddleston, J., Antonacci, F., Penewit, K., Denman, L., Raja, A., et al. (2017) · Nature Ecology & Evolution · doi:10.1038/s41559-016-0069 · Cited by 159
Contribution of thalamic input to the specification of cytoarchitectonic cortical fields in the primate: Effects of bilateral enucleation in the fetal monkey on the boundaries, dimensions, and gyrification of striate and extrastriate cortex
Dehay, C., Giroud, P., Berland, M., Killackey, H. P., & Kennedy, H. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960325)367:1 · Cited by 157
Modulation of the cell cycle contributes to the parcellation of the primate visual cortex
Dehay, C., Giroud, P., Berland, M., Smart, I. H. M., & Kennedy, H. (1993) · Nature · doi:10.1038/366464a0 · Cited by 156
Genetics of the polymicrogyria syndromes
Jansen, A., & Andermann, E. (2005) · Journal of Medical Genetics · doi:10.1136/jmg.2004.023952 · Cited by 156
Compartmentalization of Cerebral Cortical Germinal Zones in a Lissencephalic Primate and Gyrencephalic Rodent
García‐Moreno, F., Vasistha, N. A., Trévia, N., Bourne, J. A., & Molnár, Z. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr312 · Cited by 154
Genotype–phenotype analysis of human frontoparietal polymicrogyria syndromes
Piao, X., Chang, B. S., Bodell, A., Woods, K., Ben‐Zeev, B., Topçu, M., Guerrini, R., Goldberg‐Stern, H., Sztriha, L., Dobyns, W. B., et al. (2005) · Annals of Neurology · doi:10.1002/ana.20616 · Cited by 151
Gradients in the Brain: The Control of the Development of Form and Function in the Cerebral Cortex
Sansom, S. N., & Livesey, F. J. (2009) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a002519 · Cited by 148
GPR56-related bilateral frontoparietal polymicrogyria: further evidence for an overlap with the cobblestone complex
Bahi-Buisson, N., Poirier, K., Boddaert, N., Fallet-Bianco, C., Specchio, N., Bertini, E., Caglayan, O., Lascelles, K., Elie, C., Rambaud, J., et al. (2010) · Brain · doi:10.1093/brain/awq259 · Cited by 144
The Primate-Specific Gene TMEM14B Marks Outer Radial Glia Cells and Promotes Cortical Expansion and Folding
Liu, J., Liu, W., Yang, L., Wu, Q., Zhang, H., Fang, A., Li, L., Xu, X., Sun, L., Zhang, J., et al. (2017) · Cell stem cell · doi:10.1016/j.stem.2017.08.013 · Cited by 143
How Cells Fold the Cerebral Cortex
Borrell, V. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1106-17.2017 · Cited by 143
Self-citation
Regulation of Cerebral Cortex Folding by Controlling Neuronal Migration via FLRT Adhesion Molecules
del Toro, D., Ruff, T., Cederfjäll, E. A., Villalba, A., Seyit-Bremer, G., Borrell, V., & Klein, R. (2017) · Cell · doi:10.1016/j.cell.2017.04.012 · Cited by 142
Self-citation
Analysis of 17 genes detects mutations in 81% of 811 patients with lissencephaly
Donato, N. D., Timms, A. E., Aldinger, K. A., Mirzaa, G., Bennett, J. T., Collins, S., Olds, C., Mei, D., Chiari, S., Carvill, G. L., et al. (2018) · Genetics in Medicine · doi:10.1038/gim.2018.8 · Cited by 142
Scratch regulates neuronal migration onset via an epithelial-mesenchymal transition–like mechanism
Itoh, Y., Moriyama, Y., Hasegawa, T., Endo, T. A., Toyoda, T., & Gotoh, Y. (2013) · Nature Neuroscience · doi:10.1038/nn.3336 · Cited by 138
Cytomechanics of neurite outgrowth from chick brain neurons
Chada, S., Lamoureux, P. L., Buxbaum, R. E., et al. (1997) · Journal of Cell Science · doi:10.1242/jcs.110.10.1179 · Cited by 133
A restricted period for formation of outer subventricular zone defined by Cdh1 and Trnp1 levels
Martínez‐Martínez, M. Á., Romero, C. D. J., Fernández, V., Cárdenas, A., Götz, M., & Borrell, V. (2016) · Nature Communications · doi:10.1038/ncomms11812 · Cited by 133
Self-citation
How Forces Fold the Cerebral Cortex
Kroenke, C. D., & Bayly, P. V. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1105-17.2017 · Cited by 132
Order‐specific quantitative patterns of cortical gyrification
Pillay, P., & Manger, P. R. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05524.x · Cited by 130
Polymicrogyria: pathology, fetal origins and mechanisms
Squier, W., & Jansen, A. (2014) · Acta Neuropathologica Communications · doi:10.1186/s40478-014-0080-3 · Cited by 122
An Autosomal Recessive Form of Bilateral Frontoparietal Polymicrogyria Maps to Chromosome 16q12.2-21
Piao, X., Basel‐Vanagaite, L., Straussberg, R., Grant, P. E., Pugh, E., Doheny, K. F., Doan, B. Q., Hong, S. E., Shugart, Y. Y., & Walsh, C. A. (2002) · The American Journal of Human Genetics · doi:10.1086/339552 · Cited by 120
Mutations in KATNB1 Cause Complex Cerebral Malformations by Disrupting Asymmetrically Dividing Neural Progenitors
Mishra-Gorur, K., Çağlayan, A. O., Schaffer, A. E., Chabu, C. Y., Henegariu, O., Vonhoff, F., Akgumus, G. T., Nishimura, S., Han, W., Tu, S., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.12.014 · Cited by 120
Integrin αvβ3 and thyroid hormones promote expansion of progenitors in embryonic neocortex
Stenzel, D., Wilsch‐Bräuninger, M., Wong, F. K., Heuer, H., & Huttner, W. Β. (2014) · Development · doi:10.1242/dev.101907 · Cited by 118
The Transition from Radial Glial to Intermediate Progenitor Cell Is Inhibited by FGF Signaling during Corticogenesis
Kang, W., Wong, L. C., Shi, S., & Hébert, J. M. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3844-09.2009 · Cited by 118
Recessive LAMC3 mutations cause malformations of occipital cortical development
Barak, T., Kwan, K. Y., Louvi, A., Demirbilek, V., Saygı, S., Tüysüz, B., Choi, M., Boyacı, H., Doerschner, K., Zhu, Y., et al. (2011) · Nature Genetics · doi:10.1038/ng.836 · Cited by 116
Gyrus formation in the cerebral cortex in the ferret. I. Description of the external changes.
Smart, I. H. M., & McSherry, G. M. (1986) · PubMed · Cited by 113
Mouse models of human PIK3CA-related brain overgrowth have acutely treatable epilepsy
Roy, A., Skibo, J., Kalume, F. K., Ni, J., Rankin, S. L., Lu, Y., Dobyns, W. B., Mills, G. B., Zhao, J. J., Baker, S. J., et al. (2015) · eLife · doi:10.7554/elife.12703 · Cited by 113
Emerging Brain Morphologies from Axonal Elongation
Holland, M. A., Miller, K. E., & Ellen Kuhl, A. (2015) · Annals of Biomedical Engineering · doi:10.1007/s10439-015-1312-9 · Cited by 112
Cortical Gyrification Induced by Fibroblast Growth Factor 2 in the Mouse Brain
Rash, B. G., Tomasi, S., Lim, H., Suh, C. Y., & Vaccarino, F. M. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3621-12.2013 · Cited by 109
Pathological Consequences of Sequence Duplications in the Human GenomePreprint
Mazzarella, R. A., & Schlessinger, D. (1998) · Genome Research · doi:10.1101/gr.8.10.1007 · Cited by 109
De novo mutations in GRIN1 cause extensive bilateral polymicrogyria
Fry, A. E., Fawcett, K. A., Zelnik, N., Yuan, H., Thompson, B. A. N., Shemer-Meiri, L., Cushion, T. D., Mugalaasi, H., Sims, D., Stoodley, N., et al. (2017) · Brain · doi:10.1093/brain/awx358 · Cited by 105
TAG-1–assisted progenitor elongation streamlines nuclear migration to optimize subapical crowding
Okamoto, M., Namba, T., Shinoda, T., Kondo, T., Watanabe, T., Inoue, Y., Takeuchi, K., Enomoto, Y., Ota, K., Oda, K., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3525 · Cited by 103
The physical state of fibronectin matrix differentially regulates morphogenetic movements in vivo
Rozario, T., Dzamba, B. J., Weber, G. F., Davidson, L. A., & DeSimone, D. W. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.12.025 · Cited by 103
Gyrus formation in the cerebral cortex of the ferret. II. Description of the internal histological changes.
Smart, I. H. M., & McSherry, G. M. (1986) · PubMed · Cited by 102
Sustained Pax6 Expression Generates Primate-like Basal Radial Glia in Developing Mouse Neocortex
Wong, F. K., Fei, J., Mora‐Bermúdez, F., Taverna, E., Haffner, C., Fu, J., Anastassiadis, K., Stewart, A. F., & Huttner, W. Β. (2015) · PLoS Biology · doi:10.1371/journal.pbio.1002217 · Cited by 101
Residual stress in the adult mouse brain
Xu, G., Bayly, P., & Taber, L. (2008) · Biomechanics and Modeling in Mechanobiology · doi:10.1007/s10237-008-0131-4 · Cited by 100
Insights into the gyrification of developing ferret brain by magnetic resonance imaging
Neal, J., Takahashi, M., Silva, M. J., Tiao, G., Walsh, C. A., & Sheen, V. L. (2006) · Journal of Anatomy · doi:10.1111/j.1469-7580.2006.00674.x · Cited by 100
A single splice site mutation in human-specific ARHGAP11B causes basal progenitor amplification
Florio, M., Namba, T., Pääbo, S., Hiller, M., & Huttner, W. Β. (2016) · Science Advances · doi:10.1126/sciadv.1601941 · Cited by 100
Tension as a regulator and integrator of axonal growth
Heidemann, S. R., & Buxbaum, R. E. (1990) · Cell Motility and the Cytoskeleton · doi:10.1002/cm.970170103 · Cited by 97
Generation of transgenic marmosets expressing genetically encoded calcium indicators
Park, J. E., Zhang, X. F., Choi, S., Okahara, J., Sasaki, E., & Silva, A. C. (2016) · Scientific Reports · doi:10.1038/srep34931 · Cited by 97
Developmental Sculpting of Dendritic Morphology of Layer 4 Neurons in Visual Cortex: Influence of Retinal Input
Callaway, E. M., & Borrell, V. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.5222-10.2011 · Cited by 95
Self-citation
The secondary loss of gyrencephaly as an example of evolutionary phenotypical reversal
Kelava, I., Lewitus, É., & Huttner, W. Β. (2013) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2013.00016 · Cited by 93
Refining the phenotype of α‐1a Tubulin (TUBA1A) mutation in patients with classical lissencephaly
Morris-Rosendahl, D. J., Najm, J., Lachmeijer, A. M. A., et al. (2008) · Clinical Genetics · doi:10.1111/j.1399-0004.2008.01093.x · Cited by 92
Folding of the Cerebral Cortex Requires Cdk5 in Upper-Layer Neurons in Gyrencephalic Mammals
Shinmyo, Y., Terashita, Y., Duong, T. A. D., Hamabe‐Horiike, T., Kawasumi, M., Hosomichi, K., Tajima, A., & Kawasaki, H. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.08.024 · Cited by 89
ARX mutations in X-linked lissencephaly with abnormal genitalia
Uyanık, G., Aigner, L., Martin, P., et al. (2003) · Neurology · doi:10.1212/01.wnl.0000079371.19562.ba · Cited by 88
Transgenic Monkey Model of the Polyglutamine Diseases Recapitulating Progressive Neurological Symptoms
Tomioka, I., Ishibashi, H., Minakawa, E. N., Motohashi, H. H., Takayama, O., Saito, Y., Popiel, H. A., Puentes, S., Owari, K., Nakatani, T., et al. (2017) · eNeuro · doi:10.1523/eneuro.0250-16.2017 · Cited by 88
The protomap is propagated to cortical plate neurons through an Eomes -dependent intermediate map
Elsen, G. E., Hodge, R. D., Bedogni, F., Daza, R. A. M., Nelson, B. R., Shiba, N., Reiner, S. L., & Hevner, R. F. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1209076110 · Cited by 87
RTTN Mutations Link Primary Cilia Function to Organization of the Human Cerebral Cortex
Kia, S. K., Verbeek, E., Engelen, E., Schot, R., Poot, R. A., de Coo, I. F. M., Lequin, M. H., Poulton, C. J., Pourfarzad, F., Grosveld, F. G., et al. (2012) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2012.07.008 · Cited by 85
Insm1 Induces Neural Progenitor Delamination in Developing Neocortex via Downregulation of the Adherens Junction Belt-Specific Protein Plekha7
Tavano, S., Taverna, E., Kalebic, N., Haffner, C., Namba, T., Dahl, A., Wilsch‐Bräuninger, M., Paridaen, J. T. M. L., & Huttner, W. Β. (2018) · Neuron · doi:10.1016/j.neuron.2018.01.052 · Cited by 85
Neuronal Migration Dynamics in the Developing Ferret Cortex
Gertz, C. C., & Kriegstein, A. R. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.2198-15.2015 · Cited by 84
Mechanisms of brain evolution: Regulation of neural progenitor cell diversity and cell cycle length
Borrell, V., & Calegari, F. (2014) · Neuroscience Research · doi:10.1016/j.neures.2014.04.004 · Cited by 82
Self-citation
Novel primate miRNAs coevolved with ancient target genes in germinal zone-specific expression patterns
Arcila, M. L., Betizeau, M., Cambronne, X. A., Guzman, E., Doerflinger, N., Bouhallier, F., Zhou, H., Wu, B., Rani, N., Bassett, D. S., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.01.017 · Cited by 80
Gyrification of the cerebral cortex requires FGF signaling in the mammalian brain
Matsumoto, N., Shinmyo, Y., Ichikawa, Y., & Kawasaki, H. (2017) · eLife · doi:10.7554/elife.29285 · Cited by 77
The Phosphatase PP4c Controls Spindle Orientation to Maintain Proliferative Symmetric Divisions in the Developing Neocortex
Xie, Y., Jüschke, C., Esk, C., Hirotsune, S., & Knoblich, J. A. (2013) · Neuron · doi:10.1016/j.neuron.2013.05.027 · Cited by 75
Mitotic Spindle Asymmetry: A Wnt/PCP-Regulated Mechanism Generating Asymmetrical Division in Cortical Precursors
Delaunay, D., Cortay, V., Patti, D., Knoblauch, K., & Dehay, C. (2014) · Cell Reports · doi:10.1016/j.celrep.2013.12.026 · Cited by 75
Cellular and Clinical Impact of Haploinsufficiency for Genes Involved in ATR Signaling
O’Driscoll, M., Dobyns, W. B., van Hagen, J. M., & Jeggo, P. A. (2007) · The American Journal of Human Genetics · doi:10.1086/518696 · Cited by 74
The Structure of the Coiled-Coil Domain of Ndel1 and the Basis of Its Interaction with Lis1, the Causal Protein of Miller-Dieker Lissencephaly
Derewenda, U., Tarricone, C., Choi, W. C., Cooper, D. R., Lukasik, S., Perrina, F., Tripathy, A., Kim, M. H., Cafiso, D. S., Musacchio, A., et al. (2007) · Structure · doi:10.1016/j.str.2007.09.015 · Cited by 74
Polymicrogyria in chromosome 22 deletion syndrome
Bingham, P. M., Lynch, D., McDonald‐McGinn, D. M., & Zackai, E. H. (1998) · Neurology · doi:10.1212/wnl.51.5.1500 · Cited by 74
TIPs Are Tension-Responsive Proteins Involved in Myogenic versus Adipogenic Differentiation
Jakkaraju, S., Zhe, X., Pan, D., Choudhury, R., & Schuger, L. A. (2005) · Developmental Cell · doi:10.1016/j.devcel.2005.04.015 · Cited by 73
Long non‐coding RNAs in corticogenesis: deciphering the non‐coding code of the brain
Aprea, J., & Calegari, F. (2015) · The EMBO Journal · doi:10.15252/embj.201592655 · Cited by 72
TUBA1A mutations
Jansen, A., Oostra, A., Desprechins, B., et al. (2011) · Neurology · doi:10.1212/wnl.0b013e31821043f5 · Cited by 70
Megalencephaly and Perisylvian Polymicrogyria with Postaxial Polydactyly and Hydrocephalus: A Rare Brain Malformation Syndrome Associated with Mental Retardation and Seizures
Mirzaa, G., Dodge, N. N., Glass, I. A., Day, C. S., Gripp, K. W., Nicholson, L., Straub, V. W., Voït, T., & Dobyns, W. B. (2004) · Neuropediatrics · doi:10.1055/s-2004-830497 · Cited by 68
An essential role of SVZ progenitors in cortical folding in gyrencephalic mammals
Toda, T., Shinmyo, Y., Duong, T. A. D., Masuda, K., & Kawasaki, H. (2016) · Scientific Reports · doi:10.1038/srep29578 · Cited by 67
Pathophysiological analyses of cortical malformation using gyrencephalic mammals
Masuda, K., Toda, T., Shinmyo, Y., Ebisu, H., Hoshiba, Y., Wakimoto, M., Ichikawa, Y., & Kawasaki, H. (2015) · Scientific Reports · doi:10.1038/srep15370 · Cited by 66
Folding, But Not Surface Area Expansion, Is Associated with Cellular Morphological Maturation in the Fetal Cerebral Cortex
Wang, X., Studholme, C., Grigsby, P. L., Frias, A. E., Carlson, V. C. C., & Kroenke, C. D. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.3157-16.2017 · Cited by 58
Rotatin is a novel gene required for axial rotation and left-right specification in mouse embryos.
Faisst, A. M., Alvarez-Bolado, G., Treichel, D., & Gruss, P. (2002) · Mechanisms of Development · doi:10.1016/s0925-4773(02)00003-5 · Cited by 56
The Concerted Modulation of Proliferation and Migration Contributes to the Specification of the Cytoarchitecture and Dimensions of Cortical Areas
Lukaszewicz, A. I., Cortay, V., Giroud, P., Berland, M., Smart, I. H. M., Kennedy, H., & Dehay, C. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhk011 · Cited by 54
The birth of a human-specific neural gene by incomplete duplication and gene fusion
Dougherty, M. L., Nuttle, X., Penn, O., Nelson, B. J., Huddleston, J., Baker, C. A., Harshman, L., Duyzend, M., Ventura, M., Antonacci, F., et al. (2017) · Genome biology · doi:10.1186/s13059-017-1163-9 · Cited by 51
A Golgi study of the sixth layer of the cerebral cortex. II. The gyrencephalic brain of Carnivora, Artiodactyla and Primates.
Ferrer, I., Fábregues, I., & Condom, E. (1986) · PubMed · Cited by 49
Micropatterned stretching system for the investigation of mechanical tension on neural stem cells behavior
Chang, Y.-J., Tsai, C. H., Tseng, F., Chen, T.-J., & Wang, T. (2012) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2012.07.008 · Cited by 48
CRISPR/Cas9-mediated genome engineering of the ferret
Kou, Z., Wu, Q., Kou, X., Yin, C., Wang, H., Zuo, Z., Zhuo, Y., Chen, A., Gao, S., & Wang, X. (2015) · Cell Research · doi:10.1038/cr.2015.130 · Cited by 46
Reorganization of Exuberant Axonal Arbors Contributes to the Development of Laminar Specificity in Ferret Visual Cortex
Borrell, V., & Callaway, E. M. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-15-06682.2002 · Cited by 43
Self-citation
Investigation of brain science and neurological/psychiatric disorders using genetically modified non-human primates
Okano, H., & Kishi, N. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.10.016 · Cited by 40
Truncation ofNHEJ1 in a patient with polymicrogyria
Cantagrel, V., Lossi, A.-M., Lisgo, S., Missirian, C., Borges, A., Philip, N., Fernandez, C., Cardoso, C., Figarella-Branger, D. F., Moncla, A., et al. (2006) · Human Mutation · doi:10.1002/humu.20450 · Cited by 37
Cortical Ventricular Zone Progenitors and Their Progeny Maintain Spatial Relationships and Radial Patterning during Preplate Development Indicating an Early Protomap
O’Leary, D. D. M., & Borngasser, D. J. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhk019 · Cited by 37
Genetic maps and patterns of cerebral cortex folding
Romero, C. D. J., & Borrell, V. (2017) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2017.11.009 · Cited by 37
Self-citation

Research works printed but not linked: 2

Bok, S. T. Histonomy of the Cerebral Cortex (Elsevier, 1959).
Bahi-Buisson, N. & Cavallin, M. Tubulinopathies overview. GeneReviews https://www.ncbi.nlm.nih.gov/books/NBK350554 (updated 24 Mar 2016).

Sorted by citations

Development of prefrontal cortex
Kolk, S. M., & Rakic, P. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01137-9 · Cited by 378
“And if we were to focus more on the evolutionary aspects of prefrontal development in terms of structural organization and function, should we not include longitudinal neurodevelopmental studies on more species [18, 19]? Although the basic principles of cortical development may be similar in all mammals, the modificat…”
Background
Programmed and self-organized flow of information during morphogenesis
Collinet, C., & Lecuit, T. (2021) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-00318-6 · Cited by 322
MRI of the Neonatal Brain: A Review of Methodological Challenges and Neuroscientific Advances
Dubois, J., Alison, M., Counsell, S. J., Hertz‐Pannier, L., Hüppi, P. S., & Benders, M. J. N. L. (2021) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.27192 · Cited by 226
Cortical Malformations: Lessons in Human Brain Development
Subramanian, L., Calcagnotto, M. E., & Paredes, M. F. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00576 · Cited by 138
“, 2012) has led to the hypothesis that the presence of this expanded progenitor pool might be an important driver of cortical folding (Stahl et al., 2013; Wang et al., 2016; Borrell, 2018; Llinares-Benadero and Borrell, 2019).”
Background
A 2020 view of tension-based cortical morphogenesis
Essen, D. C. V. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2016830117 · Cited by 124
“In such models it is important to distinguish between “bona fide” folding (with a smooth underlying ventricular suface) and wrinkling that includes all layers of the cerebral wall (75, 109) (SI Appendix, Topic 9).”
Influential

See all 243

Authors: Llinares-Benadero, C., & Borrell, V.
Affiliations: Consejo Superior de Investigaciones Científicas (ES)
ORCID: Llinares-Benadero, Cristina
Venue: Nature Reviews Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2019-01-04
Volume: 20
Issue: 3
Pages: 161-176
ISSN: 1471-003X (ISSN-L)
1471-0048
DOI: 10.1038/s41583-018-0112-2
OpenAlex: W2907389933
Semantic Scholar: 5e11290de5ea2c272c18ac0c97260aae0579a518
Cited by: 243
References: 216
Citations by year: 2026: 24 · 2025: 16 · 2024: 52 · 2023: 44 · 2022: 27 · 2021: 33 · 2020: 36 · 2019: 11
FWCI: 3.37
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature reviews. Neuroscience (publishedVersion)
PubMed (publishedVersion)
DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
Topics: Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Fetal and Pediatric Neurological Disorders
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Keywords: cortical folding, cerebral cortex, brain evolution
MeSH terms: Animals, Cell Movement, Cerebral Cortex, Biological Evolution, Humans, Neuroglia, Neurons, Neurogenesis

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Deconstructing cortical folding: genetic, cellular and mechanical determinants

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks