365:(SVZ), amplifying the number of cortical neurons being produced. The long fibers of RGCs project all the way through the developing cortex to the pial surface of the brain, and these fibers serve as physical guides for neuronal migration. A second class of RGC, termed basal RGCs (bRGC)s, forms a third progenitor pool in the outer SVZ. Basal RGCs are generally much more abundant in higher mammals. Both classic RGCs and the recently described bRGCs represent guiding cues that lead newborn neurons to their destination in the cortex. Increased numbers of bRGCs increase the density of guiding fibers in an otherwise fanning out array which would lose fiber density. The scientific literature points to differences in the dynamics of proliferation and neuronal differentiation in each of these progenitor zones across mammalian species, and such differences may account for the large differences in cortical size and gyrification among mammals. One hypothesis suggests that certain progenitor cells generate abundant neurons destined for the outer cortical layers, causing greater surface area increase in the outer layers compared with the inner cortical layers. It remains unclear how this may work without further mechanistic elements.
520:
237:; ossification of the cranial plates does not occur until later in development. The human cranium continues to grow substantially along with the brain after birth until the cranial plates finally fuse after several years. Experimental studies in animals have furthermore shown that cortical folding can occur without external constraints. Cranial growth is thus thought to be driven by brain growth; mechanical and genetic factors intrinsic to the brain are now thought to be the primary drivers of gyrification. The only observed role that the cranium may play in gyrification is in flattening of gyri as the brain matures after the cranial plates fuse.
536:
404:. Some, like mouse brains, remain lissencephalic throughout adulthood. It has been shown that lissencephalic species possess many of the molecular cues needed to achieve gyrencephaly, but a large variety of genes are involved in the regulation of the neural progenitor proliferation and neurogenic processes that underlie gyrification. It is hypothesized that spatiotemporal differences in these molecular pathways, including FGF, Shh, and Trnp1 and likely many others, determine the timing and extent of gyrification in various species.
312:. Local expression levels of Trnp1, can determine the future position of developing folds/gyri in human brains. Genes that influence cortical progenitor dynamics, neurogenesis and neuronal migration, as well as genes that influence the development of cortical circuits and axonal projections may all contribute to gyrification. Trnp1 is a DNA-binding factor that has been shown to regulate other genes that regulate the proliferation of cortical progenitor cells – thereby serving as a master gene-regulator. In addition, the
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and generate the excitatory glutamatergic neurons of the cerebral cortex. These cells rapidly proliferate through self-renewal at early developmental stages, expanding the progenitor pool and increasing cortical surface area. At this stage, the pattern of cortical areas is genetically programmed by a
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twins of the late 1990s support this idea, particularly with regards to primary gyri and sulci, whereas there is more variability among secondary and tertiary gyri. Therefore, one may hypothesize that secondary and tertiary folds could be more sensitive to genetic and environmental factors. The first
127:
As fetal development proceeds, gyri and sulci begin to take shape with the emergence of deepening indentations on the surface of the cortex. Not all gyri begin to develop at the same time. Instead, the primary cortical gyri form first (beginning as early as gestational week 10 in humans), followed by
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and subsequent cell death. Death of cortical stem cells causes the loss of all expected daughter cells, and the scope of the malformation thus depends on the timing of infection as well as its severity during the schedule of neural stem cell proliferation and neurogenesis. Earlier infections would
281:
growth suggests that the grey (outer shell) and white matter (inner core) layers each grow at separate rates, that are uniform in all dimensions. Tangential growth suggests that the grey matter grows at a faster rate than the inner white matter and that the growth rate of the grey matter determines
268:
Early conditions of the brain have a strong influence on its final level of gyrification. In particular, there is an inverse relationship between cortical thickness and gyrification. Areas of the brain with low values of thickness are found to have higher levels of gyrification. The reverse is also
245:
An alternative theory suggests that axonal tension forces between highly interconnected cortical areas pull local cortical areas towards each other, inducing folds. This model has been criticised: A numerical computer simulation could not produce a biologically realistic folding pattern. One study
503:
Cortical
Gyrification can be measured in terms of the Gyrification Index (GI), Fractal Dimensionality and a combination of morphometric terms (Area, Thickness, Volume). The GI is defined as the ratio between the Total Area and the Exposed Area ("perimeter of the brain delineated on two-dimensional
410:
is a human disease state. For humans with lissencephaly, a large number of neurons fail to reach the outer cortex during neuronal migration, and remain under the cortical plate. This displacement results in not only defects in cortical connections, but also a thickened cortex, consistent with the
422:
is a condition in which the brain has an overly convoluted cortex. Though at the surface, the brain appears smooth with a few sulci, looking at the interior of the brain reveals a convoluted structure with a large number of secondary and tertiary folds. Brain imaging with MRI reveals a brain with
381:
brains do not show gyrification. Mammals with a high GI are generally larger than those with a low GI; for example the pilot whale and bottlenose dolphin show the highest GI values. The human brain, while larger than that of a horse, shows a similar GI. Rodents generally show the lowest GIs.
254:
More recently, the theory of differential tangential expansion has been proposed, stating that folding patterns of the brain are a result of different tangential expansion rates between different cortical areas. This is proposed to be due to areal differences in early progenitor division rates.
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The folds of autistic human brains are found to experience slight shifts in location, early in brain development. Specifically, different patterns appear in the superior frontal sulcus, Sylvian fissure, inferior frontal gyrus, superior temporal gyrus, and olfactory sulci. These areas relate to
443:
have overall higher levels of cortical gyrification, but only in the temporal, parietal, and occipital lobes, as well as part of the cingulate cortex. The higher levels of gyrification are found to relate to greater local connectivity in autistic brains, suggesting hyperconnectivity.
385:
A linear relation between mammals expressed in gyrification terms has been found by Mota & Herculano-Houzel, 2015. They suggest a model that combines morphometric measurements (Cortical
Thickness, Exposed Area, and Total Area) which could be a way to describe gyrification.
320:(SHH)-signaling pathways have recently been reported to be able to induce cortical folds, with a full complement of cortical layers, in mice that live to adulthood. These FGF and Shh factors regulate cortical stem cell proliferation and neurogenesis dynamics. Roles for
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Creases on the brain's surface are formed as a result of instability, and tangential growth models reach levels of instability that cause creasing more frequently than isotropic models. This level is called a critical point, at which, the models prefer to release
298:
The pattern of cortical gyri and sulci is not random; most of the major convolutions are conserved between individuals and are also found across species. This reproducibility may suggest that genetic mechanisms can specify the location of major gyri. Studies of
450:, which was able to induce gyrification in animal models, has been hypothesized to be associated with disorders of gyrification in some cases of autism, but a review in 2012 found only one reported case of a mutation, in a patient with Rett syndrome (not ASD).
490:, or 'small-brain'. Due to the large reduction in volume of the cerebral cortex in microcephaly, changes in gyrification are not unexpected. Studies of the mechanism of Zika malformations indicate that the principal defect is due to infection of
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Gautam, Prapti; Anstey, Kaarin J.; Wen, Wei; Sachdev, Perminder S.; Cherbuin, Nicolas (2015-07-01). "Cortical gyrification and its relationships with cortical volume, cortical thickness, and cognitive performance in healthy mid-life adults".
164:
One advantage of gyrification is thought to be increased speed of brain cell communication, since cortical folds allow for cells to be closer to one other, requiring less time and energy to transmit neuronal electrical impulses, termed
454:
working memory, emotional processing, language, and eye gaze, and their difference in location and level of gyrification when compared to a neurotypical human brain could explain some altered behaviors in autistic patients.
399:
A cerebral cortex lacking surface convolutions is said to be lissencephalic, meaning 'smooth-brained'. During embryonic development, all mammalian brains begin as lissencephalic structures derived from the
198:
in the late 19th century asserts that mechanical buckling forces due to the expanding brain tissue cause the cortical surface to fold. Many theories since have been loosely tied to this hypothesis.
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polymicrogyria to have a thin cortex, consistent with the idea that a brain with a thin cortex will have a high level of gyrification. A wide array of genes when mutated have been shown to cause
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the growth rate of the white matter. Though both methods are differential, with the cortex growing more rapidly than the subcortex, tangential growth has been suggested as a more plausible model.
2758:
Palaniyappan, Lena; Mallikarjun, Pavan; Joseph, Verghese; White, Thomas P.; Liddle, Peter F. (2011). "Folding of the
Prefrontal Cortex in Schizophrenia: Regional Differences in Gyrification".
76:
projections to and from the cortical neurons residing near the surface. Gyrification allows a larger cortical surface area and hence greater cognitive functionality to fit inside a smaller
535:
1421:
Stahl, Ronny; Walcher, Tessa; De Juan Romero, Camino; Pilz, Gregor
Alexander; Cappello, Silvia; Irmler, Martin; Sanz-Aquela, José Miguel; Beckers, Johannes; Blum, Robert (2013-04-25).
1916:
Noctor, SC; Martínez-Cerdeño, V; Ivic, L; Kriegstein, AR (February 2004). "Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases".
466:, has also been associated with structural abnormalities in the brain. A reduced cortical thickness and increased gyrification is seen similar to the changes shown in those with
194:
The mechanisms of cortical gyrification are not well understood, and several hypotheses are debated in the scientific literature. A popular hypothesis dating back to the time of
2709:
Levitt, Jennifer G.; Blanton, Rebecca E.; Smalley, Susan; Thompson, P. M.; Guthrie, Donald; McCracken, James T.; Sadoun, Tania; Heinichen, Laura; Toga, Arthur W. (2003-07-01).
1738:
Noctor, SC; Flint, AC; Weissman, TA; Dammerman, RS; Kriegstein, AR (8 February 2001). "Neurons derived from radial glial cells establish radial units in neocortex".
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generally be expected to produce a more severe malformation. The microcephaly and gyrification malformations are permanent and there are no known treatments.
233:, including the future cranium). These thin layers grow easily along with cortical expansion but eventually, the cranial mesenchyme differentiates into
1789:
Malatesta, P; Hartfuss, E; Götz, M (December 2000). "Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage".
205:
is not thought to cause gyrification. This is primarily because the primordium of the cranium during the period of fetal brain development is not yet
3005:
Zilles, Karl; Armstrong, Este; Schleicher, Axel; Kretschmann, Hans-Joachim (1988-11-01). "The human pattern of gyrification in the cerebral cortex".
2602:"Cortical morphological markers in children with autism: a structural magnetic resonance imaging study of thickness, area, volume, and gyrification"
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Wu, Kong-Yan; Zuo, Guo-Long; Li, Xiao-Feng; Ye, Qing; Deng, Yong-Qiang; Huang, Xing-Yao; Cao, Wu-Chun; Qin, Cheng-Feng; Luo, Zhen-Ge (2016-05-13).
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Mota, Bruno; Herculano-Houzel, Suzana (2015-07-03). "Cortical folding scales universally with surface area and thickness, not number of neurons".
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Hansen, DV; Lui, JH; Parker, PR; Kriegstein, AR (25 March 2010). "Neurogenic radial glia in the outer subventricular zone of human neocortex".
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Tang, Hengli; Hammack, Christy; Ogden, Sarah C.; Wen, Zhexing; Qian, Xuyu; Li, Yujing; Yao, Bing; Shin, Jaehoon; Zhang, Feiran (2016-05-05).
753:
638:
169:. There is evidence to suggest a positive relationship between gyrification and cognitive information processing speed, as well as better
373:
A 'gyrification index' (GI) has been used as a measure of the magnitude of cortical convolutions on the surface of the mammalian brain.
246:
showed that gyrification can be experimentally induced in the embryonic mouse, but at early stages in the absence of axonal connections.
3227:
695:
Rajagopalan, V; Scott, J; Habas, PA; Kim, K; Corbett-Detig, J; Rousseau, F; Barkovich, AJ; Glenn, OA; Studholme, C (23 February 2011).
353:'. Cortical neurogenesis begins to deplete the pool of progenitor cells, subject to the influences of many genetic cues such as
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There is some dispute over the growth rates through which cortical and subcortical layers of the brain develop. Purely
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2654:
Identification and functional analysis of Trnp1: a novel DNA associated protein with a key role in neurogenesis
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Kandel, Eric R.; Schwartz, James H.; Jessell, Thomas M.; Siegelbaum, Steven A.; Hudspeth, A.J., eds. (2012) .
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true, that areas of the brain with high values of thickness are found to have lower levels of gyrification.
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Nowakowski, TJ; Pollen, AA; Di Lullo, E; Sandoval-Espinosa, C; Bershteyn, M; Kriegstein, AR (5 May 2016).
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1599:"Hedgehog signaling promotes basal progenitor expansion and the growth and folding of the neocortex"
1482:"Discrete domains of gene expression in germinal layers distinguish the development of gyrencephaly"
2545:"Increased gyrification, but comparable surface area in adolescents with autism spectrum disorders"
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Rakic, P (May 1972). "Mode of cell migration to the superficial layers of fetal monkey neocortex".
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362:
346:
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secondary and tertiary gyri later in development. One of the first and most prominent sulci is the
68:, only 2–4 mm thick, at the surface of the brain. Much of the interior volume is occupied by
2803:"Expression Analysis Highlights AXL as a Candidate Zika Virus Entry Receptor in Neural Stem Cells"
1869:"FGF signaling expands embryonic cortical surface area by regulating Notch-dependent neurogenesis"
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Li, C; Xu, D; Ye, Q; Hong, S; Jiang, Y; Liu, X; Zhang, N; Shi, L; Qin, CF; Xu, Z (11 May 2016).
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Nonetheless, some rodents show gyrencephaly and a few primate species are quite lissencephalic.
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Schaer, M.; Cuadra, M.B.; Tamarit, L.; Lazeyras, F.; Eliez, S.; Thiran, J.-P. (February 2008).
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656:"Gyrus formation in the cerebral cortex in the ferret. I. Description of the external changes"
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2004:"OSVZ progenitors in the human cortex: an updated perspective on neurodevelopmental disease"
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1699:"Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9"
34:
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1359:"Increased morphological asymmetry, evolvability and plasticity in human brain evolution"
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2419:
2387:"A mechanical model predicts morphological abnormalities in the developing human brain"
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2003:
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White, Tonya; Su, Shu; Schmidt, Marcus; Kao, Chiu-Yen; Sapiro, Guillermo (2010-02-01).
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in humans, ranging from mTORopathies (e.g. AKT3) to channelopathies (sodium channels, "
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1698:
19:
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2852:"Zika Virus Disrupts Neural Progenitor Development and Leads to Microcephaly in Mice"
2232:"The (not necessarily) convoluted role of basal radial glia in cortical neurogenesis"
2107:"The (not necessarily) convoluted role of basal radial glia in cortical neurogenesis"
546:
508:, a surface reconstruction Software is one of the tools available to measure the GI.
479:
463:
407:
328:) and appropriate levels of cell death of cortical progenitors have also been found.
210:
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1988:
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idea that a brain with a thicker cortex will have a lesser degree of gyrification.
321:
69:
3178:
2950:"Zika Virus Infects Human Cortical Neural Progenitors and Attenuates Their Growth"
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1325:
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152:). Most cortical gyri and sulci begin to take shape between weeks 24 and 38 of
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1.3) Regulation of Human
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361:. RGCs generate intermediate neuronal precursors that divide further in the
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1554:
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1220:"Differential tangential expansion as a mechanism for cortical gyrification"
1025:
954:
939:"Differential tangential expansion as a mechanism for cortical gyrification"
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2670:"The Emerging Picture of Autism Spectrum Disorder: Genetics and Pathology"
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2657:(Text.PhDThesis). Ludwig-Maximilians-Universität München. pp. 86–88.
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Gómez-Robles, Aida; Hopkins, William D.; Sherwood, Chet C. (2013-06-22).
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173:. Additionally, because a large cranium requires a larger pelvis during
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Striedter, Georg F.; Srinivasan, Shyam; Monuki, Edwin S. (2015-01-01).
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are due to infection during pregnancy, and are generally classified as
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96:
92:
77:
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1316:. Adolescent Brain Development: Current Themes and Future Directions.
1134:
1119:"Axons pull on the brain, but tension does not drive cortical folding"
582:"Evolution of the neocortex: a perspective from developmental biology"
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84:
61:
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generally have none. Gyrification in some animals, for example the
103:
have extensive cortical gyri, with a few species exceptions, while
3139:"A Surface-Based Approach to Quantify Local Cortical Gyrification"
447:
428:
309:
118:
42:
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Rash, BG; Lim, HD; Breunig, JJ; Vaccarino, FM (26 October 2011).
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304:
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1539:"Cerebral cortex expansion and folding: what have we learned?"
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529:; Adult mouse; Midgestation human; Newborn human; Adult human.
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Madan, Christopher R.; Kensinger, Elizabeth A. (2016-07-01).
290:
by destabilizing and forming creases to become more stable.
33:
is the process of forming the characteristic folds of the
1267:
Bartley, AJ; Jones, DW; Weinberger, DR (February 1997).
16:
Formation of the folds of the brain's cerebral cortex
345:system of signaling centers through the process of
991:"Gyrification from constrained cortical expansion"
156:, and continue to enlarge and mature after birth.
2674:Annual Review of Pathology: Mechanisms of Disease
64:of the cerebral cortex reside in a thin layer of
995:Proceedings of the National Academy of Sciences
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775:
773:
771:
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525:Various brains. Clockwise from top left: Adult
784:"Cortical Folding: When, Where, How, and Why?"
181:, a smaller cranium is more easily delivered.
1164:
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8:
308:gene reported to influence gyrification was
746:The Human Brain during the Second Trimester
115:Gyrification during human brain development
217:cerebral cortex is several thin layers of
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2726:
2685:
2627:
2617:
2576:
2519:
2418:
2255:
2171:
2130:
2027:
1892:
1714:
1622:
1570:
1513:
1448:
1438:
1390:
1333:
1284:
1243:
1194:
1142:
1042:
1024:
1006:
962:
869:American Journal of Physical Anthropology
799:
744:Bayer, Shirley A; Altman, Joseph (2005).
720:
671:
605:
2230:Hevner, RF; Haydar, TF (February 2012).
2105:Hevner, RF; Haydar, TF (February 2012).
1597:Wang, L; Hou, S; Han, YG (23 May 2016).
18:
633:(5th ed.). New York: McGraw Hill.
572:
515:
2442:
2440:
2438:
2376:
2374:
2372:
2049:
2047:
1592:
1590:
1416:
1414:
1412:
1410:
390:Neurological disorders of gyrification
111:, continues well into postnatal life.
2277:
2275:
984:
982:
654:Smart, IH; McSherry, GM (June 1986).
201:An external growth constraint of the
185:Theories on causality in gyrification
7:
3143:IEEE Transactions on Medical Imaging
2687:10.1146/annurev-pathol-012414-040405
1961:The Journal of Comparative Neurology
1123:Journal of Biomechanical Engineering
541:Normal human adult cerebrum (left),
144:, which separates the motor cortex (
40:The peak of such a fold is called a
801:10.1146/annurev-neuro-071714-034128
2381:Budday, Silvia; Raybaud, Charles;
140:), followed by others such as the
14:
748:. Boca Raton, FL USA: CRC Press.
250:Differential tangential expansion
3191:
3074:10.1016/j.neuroimage.2016.04.029
2711:"Cortical Sulcal Maps in Autism"
534:
518:
209:(hardened into the bone through
2461:10.1146/annurev.neuro.24.1.1041
2008:Current Opinion in Neurobiology
2772:10.1016/j.biopsych.2010.12.012
1885:10.1523/jneurosci.4439-11.2011
1187:10.1523/jneurosci.3621-12.2013
713:10.1523/jneurosci.5458-10.2011
336:Cortical stem cells, known as
50:), and its trough is called a
1:
2449:Annual Review of Neuroscience
2197:Brain, Behavior and Evolution
1716:10.1016/s0092-8674(00)81476-2
788:Annual Review of Neuroscience
177:, with implied difficulty in
148:) from somatosensory cortex (
87:, gyrification begins during
3233:Embryology of nervous system
2512:10.1016/j.neuron.2018.07.052
631:Principles of Neural Science
499:Measurements of gyrification
462:A more prevalent condition,
332:Cell biological determinants
213:). The tissue covering the
1873:The Journal of Neuroscience
1326:10.1016/j.bandc.2009.10.009
1175:The Journal of Neuroscience
701:The Journal of Neuroscience
586:Nature Reviews Neuroscience
123:Human cortical development.
3254:
3228:Developmental neuroscience
3118:surfer.nmr.mgh.harvard.edu
2966:10.1016/j.stem.2016.02.016
2869:10.1016/j.stem.2016.04.017
2819:10.1016/j.stem.2016.03.012
2020:10.1016/j.conb.2012.03.006
1440:10.1016/j.cell.2013.03.027
826:Behavioural Brain Research
2619:10.1186/s13229-016-0076-x
2492:"Sodium Channel SCN3A (Na
916:10.1016/j.clp.2008.06.003
838:10.1016/j.bbr.2015.03.018
580:Rakic, P (October 2009).
355:fibroblast growth factors
72:, which consists of long
3114:"LGI - Free Surfer Wiki"
474:Zika virus malformations
369:Variation across species
314:fibroblast growth factor
3155:10.1109/tmi.2007.903576
2728:10.1093/cercor/13.7.728
2304:10.1126/science.aaa9101
1846:10.1126/science.3291116
1803:10.1242/dev.127.24.5253
1668:10.1126/science.1074192
1555:10.15252/embj.201593701
1498:10.15252/embj.201591176
1286:10.1093/brain/120.2.257
1026:10.1073/pnas.1406015111
904:Clinics in Perinatology
881:10.1002/ajpa.1330440209
160:Evolutionary advantages
3007:Anatomy and Embryology
1375:10.1098/rspb.2013.0575
340:(RGC)s, reside in the
124:
27:
2760:Biological Psychiatry
2651:Stahl, Ronny (2012).
2355:10.1093/cercor/5.1.56
2248:10.1093/cercor/bhr336
2173:10.1093/cercor/bhr312
2123:10.1093/cercor/bhr336
1973:10.1002/cne.901450105
1236:10.1093/cercor/bht082
955:10.1093/cercor/bht082
171:verbal working memory
122:
22:
2561:10.1093/brain/awt106
504:coronal sections").
23:Gyrification in the
2403:2014NatSR...4E5644B
2296:2015Sci...349...74M
2076:10.1038/nature08845
2068:2010Natur.464..554H
1918:Nature Neuroscience
1838:1988Sci...241..170R
1752:2001Natur.409..714N
1660:2002Sci...297..365C
1603:Nature Neuroscience
1314:Brain and Cognition
1080:1997Natur.385..313E
1017:2014PNAS..11112667T
1001:(35): 12667–12672.
363:subventricular zone
347:cortical patterning
190:Mechanical buckling
132:(also known as the
3019:10.1007/BF00304699
2909:10.1038/cr.2016.58
2391:Scientific Reports
1369:(1761): 20130575.
660:Journal of Anatomy
492:radial glial cells
338:radial glial cells
264:Cortical thickness
259:Mechanical factors
221:(future skin) and
125:
28:
2506:(5): 905–913.e7.
2411:10.1038/srep05644
2209:10.1159/000116500
2062:(7288): 554–561.
1549:(10): 1021–1044.
1492:(14): 1859–1874.
1135:10.1115/1.4001683
910:(3): 469–78, ix.
755:978-0-8493-1422-3
640:978-0-07-139011-8
512:Additional images
231:connective tissue
167:action potentials
150:postcentral gyrus
89:fetal development
3245:
3195:
3194:
3183:
3182:
3134:
3128:
3127:
3125:
3124:
3110:
3104:
3103:
3093:
3053:
3047:
3046:
3002:
2996:
2995:
2985:
2945:
2939:
2938:
2928:
2888:
2882:
2881:
2871:
2847:
2841:
2840:
2830:
2798:
2792:
2791:
2755:
2749:
2748:
2730:
2706:
2700:
2699:
2689:
2665:
2659:
2658:
2648:
2642:
2641:
2631:
2621:
2606:Molecular Autism
2597:
2591:
2590:
2580:
2555:(6): 1956–1967.
2540:
2534:
2533:
2523:
2487:
2481:
2480:
2455:(1): 1041–1070.
2444:
2433:
2432:
2422:
2378:
2367:
2366:
2338:
2332:
2331:
2279:
2270:
2269:
2259:
2227:
2221:
2220:
2192:
2186:
2185:
2175:
2151:
2145:
2144:
2134:
2102:
2096:
2095:
2051:
2042:
2041:
2031:
1999:
1993:
1992:
1956:
1950:
1949:
1913:
1907:
1906:
1896:
1879:(43): 15604–17.
1864:
1858:
1857:
1821:
1815:
1814:
1786:
1780:
1779:
1760:10.1038/35055553
1746:(6821): 714–20.
1735:
1729:
1728:
1718:
1694:
1688:
1687:
1643:
1637:
1636:
1626:
1594:
1585:
1584:
1574:
1543:The EMBO Journal
1534:
1528:
1527:
1517:
1486:The EMBO Journal
1477:
1471:
1470:
1452:
1442:
1418:
1405:
1404:
1394:
1354:
1348:
1347:
1337:
1305:
1299:
1298:
1288:
1264:
1258:
1257:
1247:
1215:
1209:
1208:
1198:
1181:(26): 10802–14.
1166:
1157:
1156:
1146:
1114:
1108:
1107:
1088:10.1038/385313a0
1063:
1057:
1056:
1046:
1028:
1010:
986:
977:
976:
966:
934:
928:
927:
899:
893:
892:
864:
858:
857:
820:
814:
813:
803:
779:
760:
759:
741:
735:
734:
724:
692:
686:
685:
675:
651:
645:
644:
626:
620:
619:
609:
577:
538:
522:
342:ventricular zone
288:potential energy
146:precentral gyrus
3253:
3252:
3248:
3247:
3246:
3244:
3243:
3242:
3218:
3217:
3216:
3215:
3214:
3196:
3192:
3187:
3186:
3136:
3135:
3131:
3122:
3120:
3112:
3111:
3107:
3055:
3054:
3050:
3004:
3003:
2999:
2947:
2946:
2942:
2890:
2889:
2885:
2849:
2848:
2844:
2800:
2799:
2795:
2766:(10): 974–979.
2757:
2756:
2752:
2715:Cerebral Cortex
2708:
2707:
2703:
2667:
2666:
2662:
2650:
2649:
2645:
2599:
2598:
2594:
2542:
2541:
2537:
2495:
2489:
2488:
2484:
2446:
2445:
2436:
2380:
2379:
2370:
2343:Cerebral Cortex
2340:
2339:
2335:
2290:(6243): 74–77.
2281:
2280:
2273:
2236:Cerebral Cortex
2229:
2228:
2224:
2194:
2193:
2189:
2160:Cerebral Cortex
2153:
2152:
2148:
2111:Cerebral Cortex
2104:
2103:
2099:
2053:
2052:
2045:
2001:
2000:
1996:
1958:
1957:
1953:
1915:
1914:
1910:
1866:
1865:
1861:
1832:(4862): 170–6.
1823:
1822:
1818:
1797:(24): 5253–63.
1788:
1787:
1783:
1737:
1736:
1732:
1696:
1695:
1691:
1654:(5580): 365–9.
1645:
1644:
1640:
1615:10.1038/nn.4307
1596:
1595:
1588:
1536:
1535:
1531:
1479:
1478:
1474:
1420:
1419:
1408:
1363:Proc. R. Soc. B
1356:
1355:
1351:
1307:
1306:
1302:
1266:
1265:
1261:
1224:Cerebral Cortex
1217:
1216:
1212:
1168:
1167:
1160:
1116:
1115:
1111:
1074:(6614): 313–8.
1065:
1064:
1060:
988:
987:
980:
943:Cerebral Cortex
936:
935:
931:
901:
900:
896:
866:
865:
861:
822:
821:
817:
781:
780:
763:
756:
743:
742:
738:
694:
693:
689:
653:
652:
648:
641:
628:
627:
623:
598:10.1038/nrn2719
579:
578:
574:
569:
557:
550:
539:
530:
523:
514:
501:
482:induced by the
476:
460:
437:
417:
397:
392:
371:
334:
296:
294:Genetic factors
275:
266:
261:
252:
243:
192:
187:
162:
138:Sylvian fissure
134:lateral fissure
117:
35:cerebral cortex
17:
12:
11:
5:
3251:
3249:
3241:
3240:
3235:
3230:
3220:
3219:
3197:
3190:
3189:
3188:
3185:
3184:
3149:(2): 161–170.
3129:
3105:
3048:
3013:(2): 173–179.
2997:
2960:(5): 587–590.
2954:Cell Stem Cell
2940:
2903:(6): 645–654.
2883:
2856:Cell Stem Cell
2842:
2807:Cell Stem Cell
2793:
2750:
2721:(7): 728–735.
2701:
2680:(1): 111–144.
2660:
2643:
2592:
2535:
2493:
2482:
2434:
2385:(2014-07-10).
2368:
2333:
2271:
2222:
2187:
2146:
2097:
2043:
1994:
1951:
1930:10.1038/nn1172
1908:
1859:
1816:
1781:
1730:
1689:
1638:
1586:
1529:
1472:
1433:(3): 535–549.
1406:
1349:
1300:
1259:
1230:(8): 2219–28.
1210:
1158:
1109:
1058:
978:
949:(8): 2219–28.
929:
894:
859:
815:
794:(1): 291–307.
761:
754:
736:
707:(8): 2878–87.
687:
646:
639:
621:
592:(10): 724–35.
571:
570:
568:
565:
564:
563:
556:
553:
552:
551:
543:polymicrogyria
540:
533:
531:
524:
517:
513:
510:
500:
497:
475:
472:
459:
456:
439:Patients with
436:
433:
425:Polymicrogyria
420:Polymicrogyria
416:
415:Polymicrogyria
413:
396:
393:
391:
388:
370:
367:
333:
330:
318:sonic hedgehog
295:
292:
274:
271:
265:
262:
260:
257:
251:
248:
242:
241:Axonal tension
239:
191:
188:
186:
183:
161:
158:
142:central sulcus
130:lateral sulcus
116:
113:
15:
13:
10:
9:
6:
4:
3:
2:
3250:
3239:
3236:
3234:
3231:
3229:
3226:
3225:
3223:
3212:
3211:
3210:
3204:
3200:
3180:
3176:
3172:
3168:
3164:
3160:
3156:
3152:
3148:
3144:
3140:
3133:
3130:
3119:
3115:
3109:
3106:
3101:
3097:
3092:
3087:
3083:
3079:
3075:
3071:
3067:
3063:
3059:
3052:
3049:
3044:
3040:
3036:
3032:
3028:
3024:
3020:
3016:
3012:
3008:
3001:
2998:
2993:
2989:
2984:
2979:
2975:
2971:
2967:
2963:
2959:
2955:
2951:
2944:
2941:
2936:
2932:
2927:
2922:
2918:
2914:
2910:
2906:
2902:
2898:
2897:Cell Research
2894:
2887:
2884:
2879:
2875:
2870:
2865:
2861:
2857:
2853:
2846:
2843:
2838:
2834:
2829:
2824:
2820:
2816:
2812:
2808:
2804:
2797:
2794:
2789:
2785:
2781:
2777:
2773:
2769:
2765:
2761:
2754:
2751:
2746:
2742:
2738:
2734:
2729:
2724:
2720:
2716:
2712:
2705:
2702:
2697:
2693:
2688:
2683:
2679:
2675:
2671:
2664:
2661:
2656:
2655:
2647:
2644:
2639:
2635:
2630:
2625:
2620:
2615:
2611:
2607:
2603:
2596:
2593:
2588:
2584:
2579:
2574:
2570:
2566:
2562:
2558:
2554:
2550:
2546:
2539:
2536:
2531:
2527:
2522:
2517:
2513:
2509:
2505:
2501:
2497:
2486:
2483:
2478:
2474:
2470:
2466:
2462:
2458:
2454:
2450:
2443:
2441:
2439:
2435:
2430:
2426:
2421:
2416:
2412:
2408:
2404:
2400:
2396:
2392:
2388:
2384:
2377:
2375:
2373:
2369:
2364:
2360:
2356:
2352:
2348:
2344:
2337:
2334:
2329:
2325:
2321:
2317:
2313:
2309:
2305:
2301:
2297:
2293:
2289:
2285:
2278:
2276:
2272:
2267:
2263:
2258:
2253:
2249:
2245:
2241:
2237:
2233:
2226:
2223:
2218:
2214:
2210:
2206:
2203:(3): 143–50.
2202:
2198:
2191:
2188:
2183:
2179:
2174:
2169:
2166:(2): 482–92.
2165:
2161:
2157:
2150:
2147:
2142:
2138:
2133:
2128:
2124:
2120:
2116:
2112:
2108:
2101:
2098:
2093:
2089:
2085:
2081:
2077:
2073:
2069:
2065:
2061:
2057:
2050:
2048:
2044:
2039:
2035:
2030:
2025:
2021:
2017:
2014:(5): 747–53.
2013:
2009:
2005:
1998:
1995:
1990:
1986:
1982:
1978:
1974:
1970:
1966:
1962:
1955:
1952:
1947:
1943:
1939:
1935:
1931:
1927:
1924:(2): 136–44.
1923:
1919:
1912:
1909:
1904:
1900:
1895:
1890:
1886:
1882:
1878:
1874:
1870:
1863:
1860:
1855:
1851:
1847:
1843:
1839:
1835:
1831:
1827:
1820:
1817:
1812:
1808:
1804:
1800:
1796:
1792:
1785:
1782:
1777:
1773:
1769:
1765:
1761:
1757:
1753:
1749:
1745:
1741:
1734:
1731:
1726:
1722:
1717:
1712:
1709:(3): 325–37.
1708:
1704:
1700:
1693:
1690:
1685:
1681:
1677:
1673:
1669:
1665:
1661:
1657:
1653:
1649:
1642:
1639:
1634:
1630:
1625:
1620:
1616:
1612:
1609:(7): 888–96.
1608:
1604:
1600:
1593:
1591:
1587:
1582:
1578:
1573:
1568:
1564:
1560:
1556:
1552:
1548:
1544:
1540:
1533:
1530:
1525:
1521:
1516:
1511:
1507:
1503:
1499:
1495:
1491:
1487:
1483:
1476:
1473:
1468:
1464:
1460:
1456:
1451:
1446:
1441:
1436:
1432:
1428:
1424:
1417:
1415:
1413:
1411:
1407:
1402:
1398:
1393:
1388:
1384:
1380:
1376:
1372:
1368:
1364:
1360:
1353:
1350:
1345:
1341:
1336:
1331:
1327:
1323:
1319:
1315:
1311:
1304:
1301:
1296:
1292:
1287:
1282:
1279:(2): 257–69.
1278:
1274:
1270:
1263:
1260:
1255:
1251:
1246:
1241:
1237:
1233:
1229:
1225:
1221:
1214:
1211:
1206:
1202:
1197:
1192:
1188:
1184:
1180:
1176:
1172:
1165:
1163:
1159:
1154:
1150:
1145:
1140:
1136:
1132:
1129:(7): 071013.
1128:
1124:
1120:
1113:
1110:
1105:
1101:
1097:
1093:
1089:
1085:
1081:
1077:
1073:
1069:
1062:
1059:
1054:
1050:
1045:
1040:
1036:
1032:
1027:
1022:
1018:
1014:
1009:
1004:
1000:
996:
992:
985:
983:
979:
974:
970:
965:
960:
956:
952:
948:
944:
940:
933:
930:
925:
921:
917:
913:
909:
905:
898:
895:
890:
886:
882:
878:
874:
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305:dizygotic
279:isotropic
235:cartilage
215:embryonic
154:gestation
101:ungulates
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