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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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“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]
Citations
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
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
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
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).
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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…”
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
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).”
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
“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
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 122
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 126
“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 104
“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
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 86
Self-citationHeritability 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 90
“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
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 87
“…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.”
BackgroundCellular 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
Folding brains: from development to disease modeling
Del-Valle-Anton, L., & Borrell, V. (2021) · Physiological Reviews · doi:10.1152/physrev.00016.2021 · Cited by 79
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 80
Self-citationMatsumoto, N., Tanaka, S., Hamabe‐Horiike, T., Shinmyo, Y., & Kawasaki, H. (2020) · eLife · doi:10.7554/elife.54873 · Cited by 71
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 74
“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 73
“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. K., Mangin, J., & Plaze, M. (2021) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2021.712862 · Cited by 75
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 63
“Plis de passage” Deserve a Role in Models of the Cortical Folding Process
Mangin, J., Guen, Y. L., Labra, N., Grigis, A., Frouin, V., Guevara, M., Fischer, C., Rivière, D., Hopkins, W. D., Régis, J. M., et al. (2019) · Brain Topography · doi:10.1007/s10548-019-00734-8 · Cited by 70
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 61
“…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 57
“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
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 60
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Javier‐Torrent, M., Zimmer‐Bensch, G., & Nguyen, L. (2020) · Trends in Neurosciences · doi:10.1016/j.tins.2020.10.012 · Cited by 51
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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
Oproescu, A.-M., Han, S., & Schuurmans, C. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.642016 · Cited by 54
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
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Fleiss, B., Gressèns, P., & Stolp, H. B. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.00575 · Cited by 57
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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
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 48
“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
“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., Régis, J. M., Belin, P., & Coulon, O. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.117513 · Cited by 51
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Andrews, M. G., Subramanian, L., Salma, J., & Kriegstein, A. R. (2022) · Nature reviews. Neuroscience · doi:10.1038/s41583-022-00631-3 · Cited by 47
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Roy, A., Murphy, R., Deng, M., MacDonald, J. W., Bammler, T. K., Aldinger, K. A., Glass, I. A., & Millen, K. J. (2019) · eLife · doi:10.7554/elife.45961 · Cited by 41
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Babaei, B., Fovargue, D., Lloyd, R. A., Miller, R., Jugé, L., Kaplan, M., Sinkus, R., Nordsletten, D., & Bilston, L. E. (2021) · Medical Image Analysis · doi:10.1016/j.media.2021.102212 · Cited by 41
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“…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
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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
“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
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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
“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 34
Evolving Roles of Notch Signaling in Cortical Development
Nian, F., & Hou, P. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.844410 · Cited by 33
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
“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 36
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 23
Royall, L. N., Machado, D., Jessberger, S., & Denoth‐Lippuner, A. (2023) · eLife · doi:10.7554/elife.83157 · Cited by 31
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 29
“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).”
BackgroundGenetic Mechanisms Underlying Cortical Evolution in Mammals
Franchini, L. F. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.591017 · Cited by 32
“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 23
Essen, D. C. V. (2022) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2022.06.007 · Cited by 26
“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
“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
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 24
“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
Computational models of cortical folding: A review of common approaches
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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 25
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
“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
“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 26
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 26
“…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 22
Axonal cytomechanics in neuronal development
Mutalik, S. P., & Ghose, A. (2020) · Journal of Biosciences · doi:10.1007/s12038-020-00029-2 · Cited by 21
“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 24
“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
“…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
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
“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 43
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
“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
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
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
Self-citationLenge, M., Marini, C., Canale, E., Napolitano, A., MASI, S. D., Trivisano, M., Mei, D., Longo, D., Rossi‐Espagnet, M. C., Lucenteforte, E., et al. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa177 · Cited by 17
Indirect neurogenesis in space and time
Thor, S. (2024) · Nature reviews. Neuroscience · doi:10.1038/s41583-024-00833-x · Cited by 17
“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
“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 17
Li, Z., Zhang, W., Li, C., Wang, M., Wang, S., Chen, R., & Zhang, X. (2020) · Aging · doi:10.18632/aging.103402 · Cited by 18
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
“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
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 16
“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 14
“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 14
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
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 13
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 14
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 13
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
“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
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
The Control of Cortical Folding: Multiple Mechanisms, Multiple Models
Moffat, A., & Schuurmans, C. J. (2023) · The Neuroscientist · doi:10.1177/10738584231190839 · Cited by 12
“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
“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
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
“…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.”
Cortical scaling of the neonatal brain in typical and altered development
Bonthrone, A. F., Cromb, D., Chew, A. T. M., Gal-Er, B., Kelly, C. J., Falconer, S., Arichi, T., Pushparajah, K., Simpson, J. M., Rutherford, M., et al. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2416423122 · Cited by 11
Metadata
- 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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