Deconstructing cortical folding: genetic, cellular and mechanical determinants
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.
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Modifications of developmental events during primate evolution produce quantitative and qualitative changes in cellular structure and synaptic circuitry.
“Although the basic principles of cortical development may be similar in all mammals, the modifications of developmental events during millennia of primate evolution produce not only quantitative but also qualitative changes of its cellular structure and synaptic circuitry [13, 20].”
From Development of prefrontal cortex (2022) · cites this paper as [20]
Cites
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 · see citing works
Initial sequencing and comparative analysis of the mouse genome
Mouse Genome Sequencing Consortium (2002) · Nature · doi:10.1038/nature01262 · Cited by 7,187 · see citing works
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 · see citing works
King, M.-C., & Wilson, A. C. (1975) · Science · doi:10.1126/science.1090005 · Cited by 2,815 · see citing works
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 2,651 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 1,341 · see citing works
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 · see citing works
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 1,251 · see citing works
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 1,194 · see citing works
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 1,110 · see citing works
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 · see citing works
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 1,000 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 878 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 708 · see citing works
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 · see citing works
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 · see citing works
Smart, I. H. M. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.1.37 · Cited by 687 · see citing works
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 · see citing works
Cell-cycle control and cortical development
Dehay, C., & Kennedy, H. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2097 · Cited by 655 · see citing works
Human-specific gene <i>ARHGAP11B</i> 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 · see citing works
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 631 · see citing works
Self-citationHuman-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 · see citing works
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 · see citing works
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 · see citing works
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 579 · see citing works
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 · see citing works
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 · see citing works
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 552 · see citing works
Voigt, T. B. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902890106 · Cited by 549 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 503 · see citing works
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 493 · see citing works
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 · see citing works
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 471 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Shitamukai, A., Konno, D., & Matsuzaki, F. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4773-10.2011 · Cited by 450 · see citing works
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 · see citing works
Why Does Cerebral Cortex Fissure and Fold?
Welker, W. I. (1990) · Cerebral cortex · doi:10.1007/978-1-4615-3824-0_1 · Cited by 428 · see citing works
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 428 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Pilz, D. T. (1998) · Human Molecular Genetics · doi:10.1093/hmg/7.13.2029 · Cited by 360 · see citing works
Gene Duplication: The Genomic Trade in Spare Parts
Hurles, M. E. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020206 · Cited by 359 · see citing works
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 357 · see citing works
Self-citationHuman-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 352 · see citing works
Nowakowski, T. J., Pollen, A. A., Sandoval-Espinosa, C., & Kriegstein, A. R. (2016) · Neuron · doi:10.1016/j.neuron.2016.09.005 · Cited by 346 · see citing works
A Morphogenetic Model for the Development of Cortical Convolutions
Toro, R., & Burnod, Y. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhi068 · Cited by 339 · see citing works
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 · see citing works
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 317 · see citing works
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 · see citing works
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 · see citing works
Transgenic Monkeys Produced by Retroviral Gene Transfer into Mature Oocytes
Chan, A. W. S., Chong, K., Martinovich, C., et al. (2001) · Science · doi:10.1126/science.291.5502.309 · Cited by 312 · see citing works
Role of Mechanical Factors in the Morphology of the Primate Cerebral Cortex
Hilgetag, C. C., & Barbas, H. (2006) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0020022 · Cited by 310 · see citing works
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 · see citing works
Sapir, T., Elbaum, M., & Reiner, O. (1997) · The EMBO Journal · doi:10.1093/emboj/16.23.6977 · Cited by 297 · see citing works
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 · see citing works
Morphogenesis of Growing Soft Tissues
Dervaux, J., & Amar, M. B. (2008) · Physical Review Letters · doi:10.1103/physrevlett.101.068101 · Cited by 289 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Self-citationThe 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 · see citing works
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 · see citing works
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 254 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 237 · see citing works
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 · see citing works
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 · see citing works
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 233 · see citing works
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 · see citing works
Löhmann, C., & Friauf, E. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960325)367:1 · Cited by 227 · see citing works
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 223 · see citing works
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 221 · see citing works
Self-citationRegulation 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 · see citing works
Self-citationOhashi, K., Fujiwara, S., & Mizuno, K. (2017) · The Journal of Biochemistry · doi:10.1093/jb/mvw082 · Cited by 220 · see citing works
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 212 · see citing works
Self-citationAmplification 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 210 · see citing works
Self-citationGenetic Basis of Brain Malformations
Parrini, E., Conti, V., Dobyns, W. B., & Guerrini, R. (2016) · Molecular Syndromology · doi:10.1159/000448639 · Cited by 210 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 196 · see citing works
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 · see citing works
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 190 · see citing works
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 188 · see citing works
Self-citationEmerging 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 · see citing works
Self-citationDeep 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 · see citing works
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 181 · see citing works
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 · see citing works
Reillo, I., & Borrell, V. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr284 · Cited by 177 · see citing works
Self-citationMechanical 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 · see citing works
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 174 · see citing works
Mission, J., Austin, C. P., Takahashi, T., et al. (1991) · Cerebral Cortex · doi:10.1093/cercor/1.3.221 · Cited by 174 · see citing works
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 173 · see citing works
Self-citationAspm 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 · see citing works
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 170 · see citing works
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 169 · see citing works
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 · see citing works
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 162 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Genetics of the polymicrogyria syndromes
Jansen, A., & Andermann, E. (2005) · Journal of Medical Genetics · doi:10.1136/jmg.2004.023952 · Cited by 156 · see citing works
García‐Moreno, F., Vasistha, N. A., Trévia, N., Bourne, J. A., & Molnár, Z. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr312 · Cited by 154 · see citing works
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 153 · see citing works
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 151 · see citing works
Self-citationGenotype–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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
How Cells Fold the Cerebral Cortex
Borrell, V. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1106-17.2017 · Cited by 139 · see citing works
Self-citationScratch 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 · see citing works
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 138 · see citing works
Self-citationLiu, 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 138 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 129 · see citing works
Self-citationPolymicrogyria: pathology, fetal origins and mechanisms
Squier, W., & Jansen, A. (2014) · Acta Neuropathologica Communications · doi:10.1186/s40478-014-0080-3 · Cited by 122 · see citing works
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 · see citing works
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 · see citing works
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 115 · see citing works
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 114 · see citing works
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 · see citing works
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 · see citing works
Kang, W., Wong, L. C., Shi, S., & Hébert, J. M. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3844-09.2009 · Cited by 110 · see citing works
Emerging Brain Morphologies from Axonal Elongation
Holland, M. A., Miller, K. E., & Kuhl, E. (2015) · Annals of Biomedical Engineering · doi:10.1007/s10439-015-1312-9 · Cited by 109 · see citing works
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 · see citing works
Smart, I. H. M., & McSherry, G. M. (1986) · PubMed · Cited by 104 · see citing works
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 · see citing works
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 103 · see citing works
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 102 · see citing works
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 · see citing works
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 · see citing works
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 99 · see citing works
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 98 · see citing works
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 · see citing works
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 96 · see citing works
Callaway, E. M., & Borrell, V. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.5222-10.2011 · Cited by 95 · see citing works
Self-citationGeneration 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 95 · see citing works
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 · see citing works
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 90 · see citing works
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 89 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 86 · see citing works
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 82 · see citing works
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 81 · see citing works
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 · see citing works
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 78 · see citing works
Self-citationGyrification 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 76 · see citing works
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 · see citing works
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 · see citing works
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 73 · see citing works
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 · see citing works
Xie, Y., Jüschke, C., Esk, C., Hirotsune, S., & Knoblich, J. A. (2013) · Neuron · doi:10.1016/j.neuron.2013.05.027 · Cited by 72 · see citing works
Jansen, A., Oostra, A., Desprechins, B., et al. (2011) · Neurology · doi:10.1212/wnl.0b013e31821043f5 · Cited by 70 · see citing works
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 70 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Delaunay, D., Cortay, V., Patti, D., Knoblauch, K., & Dehay, C. (2014) · Cell Reports · doi:10.1016/j.celrep.2013.12.026 · Cited by 64 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Ferrer, I., Fábregues, I., & Condom, E. (1986) · PubMed · Cited by 49 · see citing works
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 · see citing works
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 · see citing works
Borrell, V., & Callaway, E. M. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-15-06682.2002 · Cited by 43 · see citing works
Self-citationOkano, H., & Kishi, N. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.10.016 · Cited by 40 · see citing works
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 · see citing works
O’Leary, D. D. M., & Borngasser, D. J. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhk019 · Cited by 37 · see citing works
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 · see citing works
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3 of the 216 references couldn’t be matched to a known paper.
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).
Cited by
Sorted by citations
Development of prefrontal cortex
Kolk, S. M., & Rakic, P. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01137-9 · Cited by 378 · see citing works
“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…”
BackgroundProgrammed 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 · see citing works
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 · see citing works
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 131 · see citing works
“, 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).”
BackgroundA 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 · see citing works
“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).”
InfluentialThe genetic architecture of human cortical folding
van der Meer, D., Kaufmann, T., Shadrin, A. A., Makowski, C., Frei, O., Roelfs, D., Sánchez, J. M., Linden, D. E. J., Rokicki, J., de Leeuw, C., et al. (2021) · Science Advances · doi:10.1126/sciadv.abj9446 · Cited by 123 · see citing works
Advancing models of neural development with biomaterials
Roth, J. G., Huang, M. S., Li, T. L., Feig, V. R., Jiang, Y., Cui, B., Greely, H. T., Bao, Z., Pașca, S. P., & Heilshorn, S. C. (2021) · Nature reviews. Neuroscience · doi:10.1038/s41583-021-00496-y · Cited by 120 · see citing works
Mechanics in the nervous system: From development to disease
Pillai, E. K., & Franze, K. (2023) · Neuron · doi:10.1016/j.neuron.2023.10.005 · Cited by 116 · see citing works
“For a more in-depth discussion of the mechanisms and forces at play during cortex folding, please see the following excellent reviews: Llinares-Benadero and Borrell, 6 Garcia et al., 138 and Del-Valle-Anton and Borrell.”
Shaping the brain: The emergence of cortical structure and folding
Akula, S. K., Exposito-Alonso, D., & Walsh, C. A. (2023) · Developmental Cell · doi:10.1016/j.devcel.2023.11.004 · Cited by 97 · see citing works
“13,50,64 In the next subsections, we will review the mechanical forces and cellular processes underlying cortical folding and discuss how the interactions between these mechanisms form the bases for the current model of cortical folding.”
BackgroundInfluentialBio‐Inspired 3D Artificial Neuromorphic Circuits
Liu, X., Wang, F., Su, J., Zhou, Y., & Ramakrishna, S. (2022) · Advanced Functional Materials · doi:10.1002/adfm.202113050 · Cited by 82 · see citing works
Molecular and cellular evolution of corticogenesis in amniotes
Cárdenas, A., & Borrell, V. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03315-x · Cited by 82 · see citing works
Self-citationCellular and Molecular Mechanisms Linking Human Cortical Development and Evolution
Libé-Philippot, B., & Vanderhaeghen, P. (2021) · Annual Review of Genetics · doi:10.1146/annurev-genet-071719-020705 · Cited by 78 · see citing works
Heritability of individualized cortical network topography
Anderson, K. M., Ge, T., Kong, R., Patrick, L. M., Spreng, R. N., Sabuncu, M. R., Yeo, B. T. T., & Holmes, A. J. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2016271118 · Cited by 85 · see citing works
“In this context, biomechanical processes such as axonal tension, intracranial pressure, and the differential growth of cortical layers are thought to influence cortical folding (51, 66), which may in turn constrain the topography of functional networks.”
BackgroundA Deep Attentive Convolutional Neural Network for Automatic Cortical Plate Segmentation in Fetal MRI
Dou, H., Karimi, D., Rollins, C. K., Ortinau, C. M., Vasung, L., Velasco‐Annis, C., Ouaalam, A., Yang, X., Ni, D., & Gholipour, A. (2020) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2020.3046579 · Cited by 78 · see citing works
The fractal brain: scale-invariance in structure and dynamics
Grosu, G. F., Hopp, A. V., Moca, V. V., Bârzan, H., Ciuparu, A., Ercsey-Ravasz, M., Winkel, M., Linde, H., & Muresan, R. C. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac363 · Cited by 83 · see citing works
“…and Chen 2011; Cuntz et al. 2012; Stevens 2012; Ercsey-Ravasz et al. 2013; Wang and Clandinin 2016; Song et al. 2021) or mechanical constraints (Garcia et al. 2018; Llinares-Benadero and Borrell 2019; Wang et al. 2019), others could also entail certain functional consequences that are essential.”
BackgroundFolding brains: from development to disease modeling
Del-Valle-Anton, L., & Borrell, V. (2021) · Physiological Reviews · doi:10.1152/physrev.00016.2021 · Cited by 78 · see citing works
Self-citationThe regulation of cortical neurogenesis
Villalba, A., Götz, M., & Borrell, V. (2020) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2020.10.003 · Cited by 74 · see citing works
Self-citationMatsumoto, N., Tanaka, S., Hamabe‐Horiike, T., Shinmyo, Y., & Kawasaki, H. (2020) · eLife · doi:10.7554/elife.54873 · Cited by 70 · see citing works
Adherens Junctions: Guardians of Cortical Development
Veeraval, L., O’Leary, C. J., & Cooper, H. M. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00006 · Cited by 69 · see citing works
“The vast majority of these neurons are generated from the basal radial glia (intermediate progenitors) within in the subventricular zone (Striedter et al., 2015; Llinares-Benadero and Borrell, 2019).”
BackgroundBest Practices in Structural Neuroimaging of Neurodevelopmental Disorders
Backhausen, L. L., Herting, M. M., Tamnes, C. K., & Vetter, N. C. (2021) · Neuropsychology Review · doi:10.1007/s11065-021-09496-2 · Cited by 66 · see citing works
“However, more recent investigations on the development of cortical folding focus on genetic influences (AlexanderBloch et al., 2020), as well as mechanical (stiffness and elasticity), and cellular mechanisms (Llinares-Benadero & Borrell, 2019).”
BackgroundCachia, A., Borst, G., Jardri, R., Raznahan, A., Murray, G., Mangin, J. F., & Plaze, M. (2021) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2021.712862 · Cited by 51 · see citing works
Behavior and lineage progression of neural progenitors in the mammalian cortex
Lin, Y., Yang, J., Shen, Z., Ma, J., Simons, B. D., & Shi, S. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.10.017 · Cited by 62 · see citing works
“Plis de passage” Deserve a Role in Models of the Cortical Folding Process
Mangin, J., Guen, Y. L., Labra, N., et al. (2019) · Brain Topography · doi:10.1007/s10548-019-00734-8 · Cited by 62 · see citing works
The Extracellular Matrix in the Evolution of Cortical Development and Folding
Amin, S., & Borrell, V. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.604448 · Cited by 58 · see citing works
“…identified ECM components as key factors regulating the proliferation of specific types of cortical progenitors, with a direct impact on the expansion and folding of the cerebral cortex (Fietz et al., 2012; Florio and Huttner, 2014; Florio et al., 2017; Long et al., 2018; Long and Huttner, 2019).”
BackgroundSelf-citationThe Evolutionary History of Brains for Numbers
Nieder, A. (2021) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2021.03.012 · Cited by 56 · see citing works
“Human-specific gene expression patterns drive the generation of more neurons during ontogeny [76].”
Backgroundde Vareilles, H., Rivière, D., Mangin, J., & Dubois, J. (2023) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2023.101249 · Cited by 56 · see citing works
Human‐specific ARHGAP11B ensures human‐like basal progenitor levels in hominid cerebral organoids
Fischer, J., Ortuño, E. F., Marsoner, F., Artioli, A., Peters, J., Namba, T., Oegema, C. E., Huttner, W. Β., Ladewig, J., & Heide, M. (2022) · EMBO Reports · doi:10.15252/embr.202254728 · Cited by 52 · see citing works
Mechanical Forces Orchestrate Brain Development
Javier‐Torrent, M., Zimmer‐Bensch, G., & Nguyen, L. (2020) · Trends in Neurosciences · doi:10.1016/j.tins.2020.10.012 · Cited by 51 · see citing works
Proneural Genes Define Ground State Rules to Regulate Neurogenic Patterning and Cortical Folding
Han, S., Okawa, S., Wilkinson, G., Ghazale, H., Adnani, L., Dixit, R., Tavares, L., Faisal, I., Brooks, M. J., Cortay, V., et al. (2020) · Neuron · doi:10.1016/j.neuron.2021.07.007 · Cited by 50 · see citing works
Oproescu, A.-M., Han, S., & Schuurmans, C. J. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.642016 · Cited by 51 · see citing works
Nelson, B. R., Hodge, R., Daza, R., Tripathi, P. P., Arnold, S., Millen, K., & Hevner, R. (2020) · eLife · doi:10.7554/elife.53777 · Cited by 41 · see citing works
Cortical Gray Matter Injury in Encephalopathy of Prematurity: Link to Neurodevelopmental Disorders
Fleiss, B., Gressèns, P., & Stolp, H. B. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.00575 · Cited by 49 · see citing works
Localized astrogenesis regulates gyrification of the cerebral cortex
Shinmyo, Y., Saito, K., Hamabe‐Horiike, T., Kameya, N., Ando, A., Kawasaki, K., Duong, T. A. D., Sakashita, M., Roboon, J., Hattori, T., et al. (2022) · Science Advances · doi:10.1126/sciadv.abi5209 · Cited by 47 · see citing works
The Symmetry of Neural Stem Cell and Progenitor Divisions in the Vertebrate Brain
Gimeno, G. C., & Paridaen, J. T. M. L. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.885269 · Cited by 45 · see citing works
“In relatively more expanded areas of the brain such as the mammalian neocortex, a higher neuronal production per individual NSC is ensured through spindle orientation changes that underlie generation of specialized basally positioned intermediate progenitors (Uzquiano et al., 2018; Llinares-Benadero and Borrell, 2019;…”
BackgroundLiang, X., Sun, L., Liao, X., Lei, T., Xia, M., Duan, D., Zeng, Z., Li, Q., Xu, Z., Men, W., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-44863-6 · Cited by 42 · see citing works
“The coef fi cient of training error, that is, the C parameter, was selected from among 16 values [2 − 5 ,2 − 4 , … ,2 9 , 2 10 ] as in a previous study 52 .”
Plis de passage in the superior temporal sulcus: Morphology and local connectivity
Bodin, C., Pron, A., Mao, M. L., et al. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.117513 · Cited by 44 · see citing works
How mechanisms of stem cell polarity shape the human cerebral cortex
Andrews, M. G., Subramanian, L., Salma, J., & Kriegstein, A. R. (2022) · Nature reviews. Neuroscience · doi:10.1038/s41583-022-00631-3 · Cited by 44 · see citing works
PI3K-Yap activity drives cortical gyrification and hydrocephalus in mice
Roy, A., Murphy, R., Deng, M., et al. (2019) · eLife · doi:10.7554/elife.45961 · Cited by 42 · see citing works
“…FLRT1/3, filamin, have been identified, that influence the balance in adhesion-repulsion forces between migrating neurons to cause interspersed cell clustering with differential migration speed, eventually establishing the cortical sulci (Borrell, 2018; Llinares-Benadero and Borrell, 2019).”
Recent advances in understanding neocortical development
Borrell, V. (2019) · F1000Research · doi:10.12688/f1000research.20332.1 · Cited by 42 · see citing works
Self-citationNeuroethology of number sense across the animal kingdom
Nieder, A. (2021) · Journal of Experimental Biology · doi:10.1242/jeb.218289 · Cited by 42 · see citing works
Tracking single-cell evolution using clock-like chromatin accessibility loci
Xiao, Y., Jin, W., Ju, L., Fu, J., Wang, G., Yu, M., Chen, F., Qian, K., Wang, X., & Zhang, Y. (2024) · Nature Biotechnology · doi:10.1038/s41587-024-02241-z · Cited by 43 · see citing works
Magnetic Resonance Elastography Reconstruction for Anisotropic Tissues
Babaei, B., Fovargue, D., Lloyd, R. A., et al. (2021) · Medical Image Analysis · doi:10.1016/j.media.2021.102212 · Cited by 39 · see citing works
Evolution of genetic mechanisms regulating cortical neurogenesis
Espinós, A., Ortuño, E. F., Negri, E., & Borrell, V. (2022) · Developmental Neurobiology · doi:10.1002/dneu.22891 · Cited by 35 · see citing works
“…of NPCs and complexity of cortical germinal zones, as compared to the small mouse, which exerted key roles in the expansion and complexification of the cerebral cortex during evolution (Dehay & Kennedy, 2007; Llinares-Benadero & Borrell, 2019; Polioudakis et al., 2019; Taverna et al., 2014).”
BackgroundSelf-citationNeuronal guidance genes in health and diseases
Yuasa‐Kawada, J., Kinoshita-Kawada, M., Tsuboi, Y., & Wu, J. Y. (2022) · Protein & Cell · doi:10.1093/procel/pwac030 · Cited by 36 · see citing works
Diversity and evolution of cerebellar folding in mammals
Heuer, K., Traut, N., de Sousa, A. A., Valk, S. L., Clavel, J., & Toro, R. (2023) · eLife · doi:10.7554/elife.85907 · Cited by 36 · see citing works
“The folding of the cerebral cortex has been the focus of intense research, both from the perspective of neurobiology ( Borrell, 2018 ; Llinares-Benadero and Borrell, 2019 ; Fernández and Borrell, 2023 ) and physics ( Toro and Burnod, 2005 ; Tallinen et al., 2014 ; Kroenke and Bayly, 2018 ).”
BackgroundBrain organoids: Human 3D models to investigate neuronal circuits assembly, function and dysfunction
Tambalo, M., & Lodato, S. (2020) · Brain Research · doi:10.1016/j.brainres.2020.147028 · Cited by 34 · see citing works
Imaging local genetic influences on cortical folding
Alexander‐Bloch, A. F., Raznahan, A., Vandekar, S., Seidlitz, J., Lu, Z., Mathias, S. R., Knowles, E. E. M., Mollon, J., Rodrigue, A., Curran, J. E., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1912064117 · Cited by 31 · see citing works
“highly penetrant genetic mutations that disrupt both folding and cortical thickness (17).”
BackgroundGenetic map of regional sulcal morphology in the human brain from UK biobank data
Sun, B. B., Loomis, S. J., Pizzagalli, F., Shatokhina, N., Painter, J. N., Foley, C. N., Biogen Biobank Team, Sun, B. B., Tsai, E. A., Bronson, P. G., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-33829-1 · Cited by 33 · see citing works
Evolving Roles of Notch Signaling in Cortical Development
Nian, F., & Hou, P. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.844410 · Cited by 32 · see citing works
H3 acetylation selectively promotes basal progenitor proliferation and neocortex expansion
Kerimoglu, C., Pham, L., Tonchev, A. B., Sakib, M. S., Xie, Y., Sokpor, G., Ulmke, P. A., Kaurani, L., Abbas, E., Nguyen, H., et al. (2021) · Science Advances · doi:10.1126/sciadv.abc6792 · Cited by 31 · see citing works
“In agreement with previous studies ( 19 , 45 , 46 ), our findings suggest that the formation of cortical folding requires a great abundance of both bIPs and bRGs. Cortical folding can be orchestrated by several genes known to critically regulate neuronal migration ( 6 ).”
Developmental mechanisms of gyrification
Fernández, V., & Borrell, V. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102711 · Cited by 34 · see citing works
Self-citationRoots of the Malformations of Cortical Development in the Cell Biology of Neural Progenitor Cells
Ossola, C., & Kalebic, N. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.817218 · Cited by 22 · see citing works
Royall, L. N., Machado, D., Jessberger, S., & Denoth‐Lippuner, A. (2023) · eLife · doi:10.7554/elife.83157 · Cited by 28 · see citing works
Differential Patterns of Gyral and Sulcal Morphological Changes During Normal Aging Process
Lin, H.-Y., Huang, C., Chou, K., Yang, A. C., Lo, C. Z., Tsai, S., & Lin, C. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.625931 · Cited by 27 · see citing works
“The cerebrum attains its folding structures through a complex orchestrated set of systematic mechanisms including differential proliferation, mechanical buckling, and differential expansion (Richman et al., 1975; Van Essen et al., 2018; Llinares-Benadero and Borrell, 2019).”
BackgroundTranscriptional cartography integrates multiscale biology of the human cortex
Wagstyl, K., Adler, S., Seidlitz, J., Vandekar, S., Mallard, T. T., Dear, R., DeCasien, A. R., Satterthwaite, T. D., Liu, S., Vértes, P. E., et al. (2024) · eLife · doi:10.7554/elife.86933.3 · Cited by 26 · see citing works
Genetic Mechanisms Underlying Cortical Evolution in Mammals
Franchini, L. F. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.591017 · Cited by 26 · see citing works
“For excellent comprehensive reviews on the matter see (Albert and Huttner, 2015; Striedter et al., 2015; Borrell, 2018; Kroenke and Bayly, 2018; Llinares-Benadero and Borrell, 2019).”
BackgroundJanssen, J., Díaz‐Caneja, C. M., Alloza, C., Schippers, A., de Hoyos, L., Santonja, J., Gordaliza, P. M., Buimer, E. E. L., van Haren, N. E. M., Cahn, W., et al. (2020) · Schizophrenia Bulletin · doi:10.1093/schbul/sbaa131 · Cited by 25 · see citing works
Essen, D. C. V. (2022) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2022.06.007 · Cited by 26 · see citing works
“Unless radial intercalation is supplanted by a viable alternative mechanism (e.g., radially biased tension within the CGM), the RD model as currently formulated [9,104,105] would allow neurons migrating into the cortical plate to stack up radially and make CGM thicker and smaller in surface area.”
Gene regulatory landscape of cerebral cortex folding
Singh, A. P., Del-Valle-Anton, L., Romero, C. D. J., Zhang, Z., Ortuño, E. F., Mahesh, A., Espinós, A., Soler, R., Cárdenas, A., Fernández, V., et al. (2024) · Science Advances · doi:10.1126/sciadv.adn1640 · Cited by 22 · see citing works
“The cerebral cortex of humans and other large mammals displays folds and fissures, which are largely absent in species with a small cortex like mice ( 1 , 2 ).”
BackgroundMethodInfluentialSelf-citationExpansion of the neocortex and protection from neurodegeneration by in vivo transient reprogramming
Shen, Y.-R., Zaballa, S., Bech, X., Sancho‐Balsells, A., Rodríguez-Navarro, I., Cifuentes-Díaz, C., Seyit-Bremer, G., Chun, S. H., Straub, T., Abante, J., et al. (2024) · Cell stem cell · doi:10.1016/j.stem.2024.09.013 · Cited by 26 · see citing works
Imaging of the superficial white matter in health and disease
Dyken, P. C. V., KHAN, A. R., & Palaniyappan, L. K. (2024) · Imaging Neuroscience · doi:10.1162/imag_a_00221 · Cited by 23 · see citing works
“Cortical folding is beyond the scope of this article but has been reviewed elsewhere ( Llinares-Benadero & Borrell, 2019; Mangin et al., 2019).”
BackgroundQuezada, S., van de Looij, Y., Hale, N., Rana, S., Sizonenko, S. V., Gilchrist, C. P., Castillo-Meléndez, M., Tolcos, M., & Walker, D. W. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa171 · Cited by 26 · see citing works
Computational models of cortical folding: A review of common approaches
Darayi, M., Hoffman, M. E., Sayut, J., Wang, S., Demirci, N., Consolini, J., & Holland, M. A. (2021) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2021.110851 · Cited by 23 · see citing works
Omlor, W., Rabe, F., Fuchs, S., Surbeck, W., Cecere, G., Huang, G.-Y., Homan, S., Kallen, N., Georgiadis, F., Spiller, T. R., et al. (2025) · American Journal of Psychiatry · doi:10.1176/appi.ajp.20230806 · Cited by 22 · see citing works
Altered extracellular matrix structure and elevated stiffness in a brain organoid model for disease
Zur, M. K., Bhattacharya, B., Solomonov, I., Dror, S. B., Savidor, A., Levin, Y., Prior, A., Sapir, T., Harris, T., Olender, T., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-59252-w · Cited by 23 · see citing works
“To determine the mechanical effects of LIS1 mutations, we employed micro-pipette aspiration (MPA) rheology and performed creep test measurementsofbrainorganoidsfrom LIS1 +/ − andcontrolorganoidsat multiple developmental ages (days 9, 18, 35, and 70).”
Secondary loss of miR-3607 reduced cortical progenitor amplification during rodent evolution
Chinnappa, K., Cárdenas, A., Prieto‐Colomina, A., Villalba, A., Márquez-Galera, Á., Soler, R., Nomura, Y., Llorens, E., Tomasello, U., López‐Atalaya, J. P., et al. (2022) · Science Advances · doi:10.1126/sciadv.abj4010 · Cited by 22 · see citing works
“These are features greatly enhanced in the developing cerebral cortex of human, macaque, and ferret, linked to the early lateral expansion of the VZ and, later, to the abundant formation of bRGCs ( 12 – 16 ), which contribute critically to the large size of these cortices ( 13 , 25 ).”
Self-citationZarzor, M. S., Blümcke, I., & Budday, S. (2023) · eLife · doi:10.7554/elife.82925 · Cited by 24 · see citing works
Cubillos, P., Ditzer, N., Kolodziejczyk, A., Schwenk, G., Hoffmann, J., Schütze, T. M., Derihaci, R. P., Birdir, C., Köllner, J. E. M., Petzold, A., et al. (2024) · The EMBO Journal · doi:10.1038/s44318-024-00068-7 · Cited by 21 · see citing works
“…self-renewing capacities, are highly abundant in species with a large gyrencephalic neocortex, and are associated with increased neocortex size, neuron number, and cortical folding (Dehay et al, 2015; Florio and Huttner, 2014; Llinares-Benadero and Borrell, 2019; Lui et al, 2011; Zhou et al, 2023).”
Early dorsomedial tissue interactions regulate gyrification of distal neocortex
Chizhikov, V. V., Iskusnykh, I. Y., Steshina, E. Y., Fattakhov, N. S., Lindgren, A., Shetty, A. S., Roy, A., Tole, S., & Millen, K. J. (2019) · Nature Communications · doi:10.1038/s41467-019-12913-z · Cited by 21 · see citing works
Axonal cytomechanics in neuronal development
Mutalik, S. P., & Ghose, A. (2020) · Journal of Biosciences · doi:10.1007/s12038-020-00029-2 · Cited by 21 · see citing works
“Though not extensively tested, the orientation and extent of axonal tension may influence cortical folding indirectly by modulating and amplifying the folding process driven by differential cortical growth (Garcia et al. 2018; Llinares-Benadero and Borrell 2019; Richman et al. 1975; Xu et al. 2010).”
BackgroundNajas, S., Pijuan, I., Esteve‐Codina, A., Usieto, S., Martinez, J. D., Zwijsen, A., Arbonés, M. L., Martı́, E., & Dréau, G. L. (2020) · Development · doi:10.1242/dev.187005 · Cited by 21 · see citing works
“Moreover, the balance between RGC self-amplification and neurogenesis appears to be regulated by extrinsic cues emanating from the ventricular fluid, meninges, blood vessels and neighbouring cells (Llinares-Benadero and Borrell, 2019; Martynoga et al., 2012; Taverna et al., 2014).”
BackgroundDecreased cortical gyrification in major depressive disorder
Kang, Y., Kang, W., Kim, A., Tae, W., Ham, B., & Han, K. (2023) · Psychological Medicine · doi:10.1017/s0033291723001216 · Cited by 20 · see citing works
“…shared gen-etic factors in phenotypic local correlation and a strong correlation with the degree of local cortical folding suggesting a patterned genetic influences on the development of cortical folding (Alexander-Bloch et al., 2020; Llinares-Benadero & Borrell, 2019; van der Meer et al., 2021).”
BackgroundSaito, K., Okamoto, M., Watanabe, Y., Noguchi, N., Nagasaka, A., Nishina, Y., Shinoda, T., Sakakibara, A., & Miyata, T. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.09.075 · Cited by 20 · see citing works
Stress landscape of folding brain serves as a map for axonal pathfinding
Solhtalab, A., Foroughi, A. H., Pierotich, L., & Razavi, M. J. (2025) · Nature Communications · doi:10.1038/s41467-025-56362-3 · Cited by 19 · see citing works
“Collectively, recent studies have supported the crucial role of mechanics and physical forces, alongside other genetic and environmental factors, in brain folding processes 21,68 – 70 .”
Transcriptional cartography integrates multiscale biology of the human cortex
Wagstyl, K., Adler, S., Seidlitz, J., Vandekar, S., Mallard, T. T., Dear, R., DeCasien, A. R., Satterthwaite, T. D., Liu, S., Vértes, P. E., et al. (2023) · eLife · doi:10.7554/elife.86933 · Cited by 42 · see citing works
Forceful patterning: theoretical principles of mechanochemical pattern formation
Rombouts, J., Elliott, J., & Erzberger, A. (2023) · EMBO Reports · doi:10.15252/embr.202357739 · Cited by 17 · see citing works
“The formation of folds is important in many systems, including the gut (Savin et al , 2011; Shyer et al , 2013), the wrinkles of the brain (Llinares-Benadero & Borrell, 2019), the development of the Drosophila wing (Tozluo ˘ glu et al , 2019), and others (see Nelson, 2016, for a review).”
BackgroundNam, K. H., Yi, S. A., Jang, H. J., Han, J., & Lee, J. (2020) · Archives of Pharmacal Research · doi:10.1007/s12272-020-01260-z · Cited by 17 · see citing works
Role of NDE1 in the Development and Evolution of the Gyrified Cortex
Soto‐Perez, J., Baumgartner, M., & Kanadia, R. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.617513 · Cited by 17 · see citing works
MiRNAs in early brain development and pediatric cancer
Prieto‐Colomina, A., Fernández, V., Chinnappa, K., & Borrell, V. (2021) · BioEssays · doi:10.1002/bies.202100073 · Cited by 17 · see citing works
Self-citationLenge, M., Marini, C., Canale, E., et al. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa177 · Cited by 17 · see citing works
Indirect neurogenesis in space and time
Thor, S. (2024) · Nature reviews. Neuroscience · doi:10.1038/s41583-024-00833-x · Cited by 16 · see citing works
“However, the development of the specific pattern of sulci and gyri of the cortex is unlikely to be solely driven by increased indirect neurogenesis, and is likely to require other molecular ‘folding instructions’ 118,260,261 .”
Kalebic, N., & Namba, T. (2021) · Development · doi:10.1242/dev.199417 · Cited by 16 · see citing works
“It is widely accepted that the increased proliferative capacity of BPs, and bRG in particular, is the key requirement for the evolutionary expansion of the neocortex, because it underlies the increase in the production of projection neurons (Kalebic and Huttner, 2020; Llinares-Benadero and Borrell, 2019; Lui et al., 2…”
BackgroundEpigenetic and metabolic regulation of developmental timing in neocortex evolution
Aquilino, M., Ditzer, N., Namba, T., & Albert, M. (2025) · Trends in Neurosciences · doi:10.1016/j.tins.2025.03.001 · Cited by 16 · see citing works
Li, Z., Zhang, W., Li, C., Wang, M., Wang, S., Chen, R., & Zhang, X. (2020) · Aging · doi:10.18632/aging.103402 · Cited by 17 · see citing works
The Mechanics of Building Functional OrgansPreprint
Andrews, T. G. R., & Priya, R. (2024) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a041520 · Cited by 15 · see citing works
“Cortical folding is one of most striking architectural features of mammalian brains and has been associated with improved neural processing power (Striedter et al. 2015; Llinares-Benadero and Borrell 2019).”
Consistency and variation in the placement of cortical folds: A perspective
Demirci, N., Jafarabadi, F., Wang, X., Wang, S., & Holland, M. A. (2023) · Brain Multiphysics · doi:10.1016/j.brain.2023.100080 · Cited by 14 · see citing works
Human brain organoid: trends, evolution, and remaining challenges
Li, M., Yuan, Y., Hou, Z., Hao, S., Jin, L., & Wang, B. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.390972 · Cited by 15 · see citing works
“Previous evidence has shown that genetic, cell biological, and biomechanical factors are critical in the complex and multifaceted process of cerebral cortical folding (Albert and Huttner, 2015; Florio et al., 2015; Del Toro et al., 2017; Borrell, 2018; Llinares-Benadero and Borrell, 2019).”
Xing, Y., Zan, C., & Liu, L. (2023) · Frontiers in Neural Circuits · doi:10.3389/fncir.2023.1007755 · Cited by 16 · see citing works
“Due to the size and the intricate folding, the cerebral cortex takes a predominant place in the brain among species (Fernández et al., 2016; Llinares-Benadero and Borrell, 2019; Bhattacharjee et al., 2021).”
BackgroundDisruption of the gene regulatory programme in neurodevelopmental disorders
Griffin, A., Mahesh, A., & Tiwari, V. K. (2022) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2022.194860 · Cited by 13 · see citing works
Automatic recognition of specific local cortical folding patterns
Borne, L., Rivière, D., Cachia, A., Roca, P., Mellerio, C., Oppenheim, C., & Mangin, J. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.118208 · Cited by 13 · see citing works
Cortical folding correlates to aging and Alzheimer’s Disease’s cognitive and CSF biomarkers
de Moraes, F. H. P., Sudo, F. K., Monteiro, M., de Melo, B. R. P., Mattos, P., Mota, B., & Tovar-Moll, F. F. (2024) · Scientific Reports · doi:10.1038/s41598-023-50780-3 · Cited by 12 · see citing works
Evolutionary changes leading to efficient glymphatic circulation in the mammalian brain
Kameya, N., Sakai, I., Saito, K., Hamabe‐Horiike, T., Shinmyo, Y., Nakada, M., Okuda, S., & Kawasaki, H. (2024) · Nature Communications · doi:10.1038/s41467-024-54372-1 · Cited by 12 · see citing works
Physiological Rules of Endocannabinoid Action During Fetal and Neonatal Brain Development
Harkany, T., & Cinquina, V. (2021) · Cannabis and Cannabinoid Research · doi:10.1089/can.2021.0096 · Cited by 12 · see citing works
Shinmyo, Y., Hamabe‐Horiike, T., Saito, K., & Kawasaki, H. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.847159 · Cited by 11 · see citing works
“One of the striking structural features of the human cerebral cortex is the large number of folds on its surface (Lui et al., 2011; Florio and Huttner, 2014; Sun and Hevner, 2014; Kawasaki, 2017; Llinares-Benadero and Borrell, 2019).”
BackgroundThe roles of inter-tissue adhesion in development and morphological evolution
Smith, S. J., Guillon, E., & Holley, S. A. (2022) · Journal of Cell Science · doi:10.1242/jcs.259579 · Cited by 11 · see citing works
de Vareilles, H., Rivière, D., Pascucci, M., Sun, Z.-Y., Fischer, C., Leroy, F., Tataranno, M. L., Benders, M. J. N. L., Dubois, J., & Mangin, J. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhac533 · Cited by 11 · see citing works
The Control of Cortical Folding: Multiple Mechanisms, Multiple Models
Moffat, A., & Schuurmans, C. J. (2023) · The Neuroscientist · doi:10.1177/10738584231190839 · Cited by 12 · see citing works
“Since bRG also preferentially generate upper-layer neurons, unsurprisingly, the resulting gyri are larger and more exaggerated in upper layers of the cortex (Llinares-Benadero and Borrell 2019).”
InfluentialMulti-scale measurement of stiffness in the developing ferret brain
Walter, C., Balouchzadeh, R., Garcia, K., Kroenke, C. D., Pathak, A., & Bayly, P. V. (2023) · Scientific Reports · doi:10.1038/s41598-023-47900-4 · Cited by 11 · see citing works
“These stiffness changes are coincident with documented increased production of ECM proteins and cell differentiation and proliferation in the brain 53,54 .”
Determinative scrolling and folding of membranes through shrinking channels
Wang, Y. Q., Wang, S., Gao, Y., Li, P., Zhao, B., Liu, S., Ma, J., Wang, L. N., Yin, Q., Wang, Z., et al. (2024) · Science Advances · doi:10.1126/sciadv.adm7737 · Cited by 11 · see citing works
Snyder, W. E., Vértes, P. E., Kyriakopoulou, V., Wagstyl, K., Williams, L. Z. J., Moraczewski, D., Thomas, A. G., Karolis, V. R., Seidlitz, J., Rivière, D., et al. (2024) · Neuron · doi:10.1016/j.neuron.2024.07.023 · Cited by 14 · see citing works
“…possible—although less likely—that the stereotyped location of linear sulci is aligned with but not caused by cytoarchitec-tonic differences, or is itself a mechanism by which cytoarchitec-tonic differences are achieved between neighboring cortical regions, 10,64 requiring further investigation.”
- Authors
- Llinares-Benadero, C., & Borrell, V.
- Affiliations
- Consejo Superior de Investigaciones Científicas (ES)
- Venue
- Nature Reviews Neuroscience
- Published
- 2019-01-04
- Volume
- 20
- Issue
- 3
- Pages
- 161-176
- ISSN
- 1471-003X (ISSN-L)
- 1471-0048
- 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
- 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
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