Frontal cortex subdivision patterning is coordinately regulated by Fgf8, Fgf17, and Emx2
Open accessAbstract
The frontal cortex (FC) plays a major role in cognition, movement and behavior. However, little is known about the genetic mechanisms that govern its development. We recently described a panel of gene expression markers that delineate neonatal FC subdivisions and identified FC regionalization defects in Fgf17–/– mutant mice (Cholfin and Rubenstein [2007] Proc. Natl. Acad. Sci. U. S. A. [in press]). In the present study, we applied this FC gene expression panel to examine regionalization phenotypes in Fgf8neo/neo, Emx2–/–, and Emx2–/–;Fgf17–/– newborn mice. We report that Fgf8, Fgf17 and Emx2 play distinct roles in the molecular regionalization of FC subdivisions. The changes in regionalization are presaged by differential effects of rostral patterning center Fgf8 and Fgf17 signaling on the rostral cortical neuroepithelium, revealed by altered expression of Spry1, Spry2, and “rostral” transcription factors Er81, Erm, Pea3, and Sp8. We used Emx2–/–;Fgf17–/– double mutants to provide direct evidence that Emx2 and Fgf17 antagonistically regulate the expression of Erm, Pea3, and Er81 in the rostral cortical neuroepithelium and FC regionalization. We have integrated our results to propose a model for how fibroblast growth factors regulate FC patterning through regulation of regional transcription factor expression within the FC anlage. J. Comp. Neurol. 509:144–155, 2008. © 2008 Wiley‐Liss, Inc.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The PFC can expand differentially and independently of the growth rate of other cortical areas.
“Work of Cholfin and Rubenstein in mice provide experimental evidence that the PFC can expand differentially and independently of the growth rate of the other areas [30, 31]”
From Development of prefrontal cortex (2022) · cites this paper as [30]
The Results section (‘Abnormal FC molecular properties in cortical patterning mutants’; page unavailable) reports changes in frontal-cortex subdivisions alongside shifts in parietal-cortex markers. The Discussion (‘Fgf17–Emx2 interactions antagonistically regulate FC patterning’; page unavailable) suggests that individual cortical areas may selectively change in size. This supports differential changes in area size, but the paper does not establish that prefrontal expansion occurs independently of other areas’ growth rates. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Specification of Cerebral Cortical Areas
Rakic, P. (1988) · Science · doi:10.1126/science.3291116 · Cited by 3,127 · see citing works
The Prefrontal Cortex—An Update
Fuster, J. M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00285-9 · Cited by 1,760 · see citing works
Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates
Dalley, J. W., Cardinal, R. N., & Robbins, T. W. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.09.006 · Cited by 1,329 · see citing works
The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat
Krettek, J. E., & Price, J. L. (1977) · The Journal of Comparative Neurology · doi:10.1002/cne.901710204 · Cited by 1,277 · see citing works
Crossley, P. H., & Martin, G. R. (1995) · Development · doi:10.1242/dev.121.2.439 · Cited by 1,177 · see citing works
An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination
Meyers, E., Lewandoski, M., & Martin, G. (1998) · Nature Genetics · doi:10.1038/ng0298-136 · Cited by 1,126 · see citing works
Do rats have a prefrontal cortex?
Uylings, H. B. M., Groenewegen, H. J., & Kolb, B. (2003) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.09.028 · Cited by 1,013 · see citing works
Heidbreder, C. A., & Groenewegen, H. J. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2003.09.003 · Cited by 882 · see citing works
Neocortex Patterning by the Secreted Signaling Molecule FGF8
Fukuchi-Shimogori, T., & Grove, E. (2001) · Science · doi:10.1126/science.1064252 · Cited by 707 · see citing works
Patterning and plasticity of the cerebral cortex
Sur, M., & Rubenstein, J. L. R. (2005) · Science · doi:10.1126/science.1112070 · Cited by 677 · see citing works
Self-citationMechanisms of Cortical Development: A View From Mutations in Mice
Caviness, V. S., & RAKIC, P. T. (1978) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.01.030178.001501 · Cited by 653 · see citing works
Regulation of Area Identity in the Mammalian Neocortex by Emx2 and Pax6
Bishop, K. M., Goudreau, G., & O’Leary, D. D. M. (2000) · Science · doi:10.1126/science.288.5464.344 · Cited by 575 · see citing works
Spine growth precedes synapse formation in the adult neocortex in vivo
Knott, G. W., Holtmaat, A., Wilbrecht, L., Welker, E., & Svoboda, K. (2006) · Nature Neuroscience · doi:10.1038/nn1747 · Cited by 563 · see citing works
Schuurmans, C. J., Gradwohl, G., Morin, X., Dierich, A., LeMeur, M., Goridis, C., & Guillemot, F. (1998) · Neuron · doi:10.1016/s0896-6273(00)80989-7 · Cited by 444 · see citing works
Hyperproliferation and Defects in Epithelial Polarity upon Conditional Ablation of α-Catenin in Skin
Vasioukhin, V., Bauer, C., Degenstein, L., Wise, B., & Fuchs, E. (2001) · Cell · doi:10.1016/s0092-8674(01)00246-x · Cited by 435 · see citing works
Genetic control of dorsal-ventral identity in the telencephalon: opposing roles for Pax6 and Gsh2
Toresson, H., Potter, S. S., & Campbell, K. (2000) · Development · doi:10.1242/dev.127.20.4361 · Cited by 387 · see citing works
Dose-dependent functions of Fgf8 in regulating telencephalic patterning centers
Storm, E. E., Garel, S., Borello, U., Hébert, J. M., Martı́nez, S., McConnell, S. K., Martin, G. R., & Rubenstein, J. L. R. (2006) · Development · doi:10.1242/dev.02324 · Cited by 361 · see citing works
Self-citationEarly Neocortical Regionalization in the Absence of Thalamic Innervation
Miyashita-Lin, E. M., Hevner, R., Wassarman, K. M., Martinez, S., & Rubenstein, J. L. R. (1999) · Science · doi:10.1126/science.285.5429.906 · Cited by 349 · see citing works
Self-citationPatterning of the Dorsal Telencephalon and Cerebral Cortex by a Roof Plate-Lhx2 Pathway
Monuki, E. S., Porter, F. D., & Walsh, C. A. (2001) · Neuron · doi:10.1016/s0896-6273(01)00504-9 · Cited by 294 · see citing works
O’Leary, D. D. M., & Nakagawa, Y. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00285-4 · Cited by 277 · see citing works
Crossley, P. H., Martı́nez, S., Ohkubo, Y., & Rubenstein, J. L. R. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00411-0 · Cited by 265 · see citing works
Self-citationXu, Z. L. J., & Ornitz, D. M. (2000) · Development · doi:10.1242/dev.127.9.1833 · Cited by 264 · see citing works
Bishop, K. M., Rubenstein, J. L. R., & O’Leary, D. D. M. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-17-07627.2002 · Cited by 260 · see citing works
Self-citationG ENERATING THE C EREBRAL C ORTICAL A REA M AP
Grove, E. A., & Shimogori, T. (2003) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.041002.131137 · Cited by 254 · see citing works
Area identity shifts in the early cerebral cortex of Emx2−/− mutant mice
Mallamaci, A., Muzio, L., Chan, C. H., Parnavelas, J. G., & Boncinelli, E. (2000) · Nature Neuroscience · doi:10.1038/76630 · Cited by 253 · see citing works
Molecular regionalization of the neocortex is disrupted inFgf8hypomorphic mutants
Garel, S., Huffman, K. J., & Rubenstein, J. L. R. (2003) · Development · doi:10.1242/dev.00416 · Cited by 249 · see citing works
Self-citationCOUP-TFI regulates the balance of cortical patterning between frontal/motor and sensory areas
Armentano, M., Chou, S., Tomassy, G. S., Leingärtner, A., O’Leary, D. D. M., & Studer, M. (2007) · Nature Neuroscience · doi:10.1038/nn1958 · Cited by 247 · see citing works
Development and decision-making in the mammalian cerebral cortex
McConnell, S. K. (1988) · Brain Research Reviews · doi:10.1016/0165-0173(88)90002-1 · Cited by 243 · see citing works
Dentate gyrus formation requires Emx2
Pellegrini, M., Mansouri, A., Simeone, A., Boncinelli, E., & Gruss, P. (1996) · Development · doi:10.1242/dev.122.12.3893 · Cited by 242 · see citing works
Hamasaki, T., Leingärtner, A., Ringstedt, T., & O’Leary, D. D. M. (2004) · Neuron · doi:10.1016/j.neuron.2004.07.016 · Cited by 234 · see citing works
Genetic Control of Cortical Regionalization and Connectivity
Rubenstein, J. L. R. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.6.524 · Cited by 224 · see citing works
Self-citationMaruoka, Y., Ohbayashi, N., Hoshikawa, M., Itoh, N., Hogan, B. L. M., & Furuta, Y. (1998) · Mechanisms of Development · doi:10.1016/s0925-4773(98)00061-6 · Cited by 200 · see citing works
Emx2 patterns the neocortex by regulating FGF positional signaling
Shimogori, T., & Grove, E. A. (2003) · Nature Neuroscience · doi:10.1038/nn1093 · Cited by 195 · see citing works
Wnt and Bmp signalling cooperatively regulate gradedEmx2 expression in the dorsal telencephalon
Theil, T., Aydin, S., Koch, S., Grotewold, L., & Rüther, U. (2002) · Development · doi:10.1242/dev.129.13.3045 · Cited by 189 · see citing works
COUP-TFI: an intrinsic factor for early regionalization of the neocortexPreprint
Zhou, C. J., Tsai, S. Y., & Tsai, M. (2001) · Genes & Development · doi:10.1101/gad.913601 · Cited by 184 · see citing works
Storm, E. E., Rubenstein, J. L. R., & Martin, G. R. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0337736100 · Cited by 181 · see citing works
Self-citationKawakami, Y., Esteban, C. R., Matsui, T., Rodríguez-León, J., Kato, S., & Belmonte, J. C. (2004) · Development · doi:10.1242/dev.01331 · Cited by 172 · see citing works
Emx2 and Pax6 Control Regionalization of the Pre-neuronogenic Cortical Primordium
Muzio, L., Benedetto, B. D., Stoykova, A., Boncinelli, E., Gruss, P., & Mallamaci, A. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.2.129 · Cited by 172 · see citing works
Expression of members of the Fgf family and their receptors during midfacial development
Bachler, M., & Neubüser, A. (2001) · Mechanisms of Development · doi:10.1016/s0925-4773(00)00518-9 · Cited by 170 · see citing works
Conversion of cerebral cortex into basal ganglia in Emx2−/− Pax6Sey/Sey double-mutant mice
Muzio, L., Benedetto, B. D., Stoykova, A., Boncinelli, E., Gruß, P., & Mallamaci, A. (2002) · Nature Neuroscience · doi:10.1038/nn892 · Cited by 159 · see citing works
Shinya, M., Koshida, S., Sawada, A., Kuroiwa, A., & Takeda, H. (2001) · Development · doi:10.1242/dev.128.21.4153 · Cited by 157 · see citing works
Patterning of frontal cortex subdivisions by Fgf17
Cholfin, J. A., & Rubenstein, J. L. R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702225104 · Cited by 154 · see citing works
Self-citationDual Role of Brain Factor-1 in Regulating Growth and Patterning of the Cerebral Hemispheres
Dou, C.-L. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.6.543 · Cited by 152 · see citing works
Expression of Sprouty genes 1, 2 and 4 during mouse organogenesis.
Zhang, S., Lin, Y.-F., Itäranta, P., Yagi, A., & Vainio, S. (2001) · Mechanisms of Development · doi:10.1016/s0925-4773(01)00526-3 · Cited by 147 · see citing works
Bishop, K. M., Garel, S., Nakagawa, Y., Rubenstein, J. L. R., & O’Leary, D. D. M. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10550 · Cited by 140 · see citing works
Self-citationFaedo, A., Tomassy, G. S., Ruan, Y., Teichmann, H., Krauss, S. J. K., Pleasure, S. J., Tsai, S. Y., Tsai, M., Studer, M., & Rubenstein, J. L. R. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm238 · Cited by 140 · see citing works
Self-citationDlx-Dependent and -Independent Regulation of Olfactory Bulb Interneuron Differentiation
Long, J. E., Garel, S., Álvarez‐Dolado, M., Yoshikawa, K., Osumi, N., Álvarez-Buylla, A., & Rubenstein, J. L. R. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.5265-06.2007 · Cited by 131 · see citing works
Self-citationOike, Y., Yasunaga, K., Ito, Y., Matsumoto, S.-I., Maekawa, H., Morisada, T., Arai, F., Nakagata, N., Takeya, M., Masuho, Y., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1531901100 · Cited by 130 · see citing works
Sp8 is crucial for limb outgrowth and neuropore closure
Bell, S. M., Schreiner, C. M., Waclaw, R. R., Campbell, K., Potter, S. S., & Scott, W. J. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2134310100 · Cited by 129 · see citing works
Sahara, S., Kawakami, Y., Belmonte, J. C. I., & O’Leary, D. D. M. (2007) · Neural Development · doi:10.1186/1749-8104-2-10 · Cited by 129 · see citing works
Bulchand, S., Subramanian, L., & Tole, S. (2003) · Developmental Dynamics · doi:10.1002/dvdy.10235 · Cited by 124 · see citing works
Genomic structure, mapping, activity and expression of fibroblast growth factor 17
Xu, J., Lawshé, A., MacArthur, C. A., & Ornitz, D. M. (1999) · Mechanisms of Development · doi:10.1016/s0925-4773(99)00034-9 · Cited by 117 · see citing works
Abnormal social behaviors in mice lacking Fgf17
Scearce-Levie, K. A., Roberson, E. D., Gerstein, H. C., Cholfin, J. A., Mandiyan, V. S., Shah, N. M., Rubenstein, J. L. R., & Mucke, L. (2007) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2007.00357.x · Cited by 113 · see citing works
Self-citationGenetic interplay between the transcription factors Sp8 and Emx2 in the patterning of the forebrain
Zembrzycki, A., Griesel, G., Stoykova, A., & Mansouri, A. (2007) · Neural Development · doi:10.1186/1749-8104-2-8 · Cited by 108 · see citing works
Emx1, Emx2 and Pax6 in Specification, Regionalization and Arealization of the Cerebral Cortex
Muzio, L. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.6.641 · Cited by 106 · see citing works
Hoshikawa, M., Ohbayashi, N., Yonamine, A., Konishi, M., Ozaki, K., Fukui, S., & Itoh, N. (1998) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1998.8239 · Cited by 103 · see citing works
Emx1 and Emx2 cooperate in initial phase of archipallium development
Shinozaki, K., Yoshida, M., Nakamura, M., Aizawa, S., & Suda, Y. (2004) · Mechanisms of Development · doi:10.1016/j.mod.2004.03.013 · Cited by 75 · see citing works
Muzio, L., Soria, J. M., Pannese, M., Piccolo, S., & Mallamaci, A. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhi077 · Cited by 75 · see citing works
Study of Fgf15 gene expression in developing mouse brain
Gimeno, L. (2003) · Gene Expression Patterns · doi:10.1016/s1567-133x(03)00059-0 · Cited by 59 · see citing works
5 Patterning of the Cerebral Cortex
Garel, S., & Rubenstein, J. L. R. (2004) · Cited by 2 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 2
- Price JL Moldin SOR Rubenstein JL Prefrontal cortex 2006 Boca Raton, FL CRC Press 526
- Zilles K Wree A Paxinos G Cortex: areal and laminar structure 1995 San Diego Academic Press 649 685
Cited by
Sorted by citations
Evolution of the neocortex: a perspective from developmental biology
Rakic, P. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2719 · Cited by 1,565 · 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
Cortical Evolution: Judge the Brain by Its Cover
Geschwind, D. H., & Rakic, P. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.045 · Cited by 519 · see citing works
New insights into the development of the human cerebral cortex
Molnár, Z., Clowry, G. J., Šestan, N., Alzu’bi, A., Bakken, T. E., Hevner, R. F., Hüppi, P. S., Kostović, I., RAKIC, P. T., Anton, E. S., et al. (2019) · Journal of Anatomy · doi:10.1111/joa.13055 · Cited by 401 · see citing works
Development of prefrontal cortex
Kolk, S. M., & Rakic, P. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01137-9 · Cited by 378 · see citing works
“Work of Cholfin and Rubenstein in mice provide experimental evidence that the PFC can expand differentially and independently of the growth rate of the other areas [30, 31] and that its size can be regulated at early stages by the change of expression of specific growth factors before they receive the afferent axonal…”
BackgroundDecision by division: making cortical maps
RAKIC, P. T., Ayoub, A. E., Breunig, J. J., & Dominguez, M. H. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2009.01.007 · Cited by 272 · see citing works
The neuroanatomy of autism – a developmental perspective
Donovan, A. P. A., & Basson, M. A. (2016) · Journal of Anatomy · doi:10.1111/joa.12542 · Cited by 266 · see citing works
Tabarés-Seisdedos, R., & Rubenstein, J. L. R. (2009) · Molecular Psychiatry · doi:10.1038/mp.2009.2 · Cited by 225 · see citing works
Self-citationThree hypotheses for developmental defects that may underlie some forms of autism spectrum disorder
Rubenstein, J. L. (2010) · Current Opinion in Neurology · doi:10.1097/wco.0b013e328336eb13 · Cited by 230 · see citing works
Self-citationFrom Cradle to Grave: The Multiple Roles of Fibroblast Growth Factors in Neural Development
Guillemot, F., & Zimmer, C. (2011) · Neuron · doi:10.1016/j.neuron.2011.08.002 · Cited by 235 · see citing works
Rubenstein, J. L. R. (2010) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2010.02307.x · Cited by 170 · see citing works
Self-citationFaedo, A., Borello, U., & Rubenstein, J. L. R. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0307-10.2010 · Cited by 170 · see citing works
Self-citationRegulation of prefrontal patterning and connectivity by retinoic acid
Shibata, M., Pattabiraman, K., Lorente-Galdós, B., Andrijević, D., Kim, S., Kaur, N., Muchnik, S. K., Xing, X., Santpere, G., Sousa, A. M. M., et al. (2021) · Nature · doi:10.1038/s41586-021-03953-x · Cited by 162 · 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
Schubert, D., Martens, G. J. M., & Kolk, S. M. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.147 · Cited by 149 · see citing works
Won, H., Huang, J. I., Opland, C. K., Hartl, C., & Geschwind, D. H. (2019) · Nature Communications · doi:10.1038/s41467-019-10248-3 · Cited by 139 · see citing works
Genes and signaling events that establish regional patterning of the mammalian forebrain
Hoch, R. V., Rubenstein, J. L. R., & Pleasure, S. (2009) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2009.02.005 · Cited by 147 · see citing works
Self-citationFGF15 promotes neurogenesis and opposes FGF8 function during neocortical development
Borello, U., Cobos, I., Long, J. E., Murre, C., & Rubenstein, J. (2008) · Neural Development · doi:10.1186/1749-8104-3-17 · Cited by 151 · see citing works
Self-citationJen, Y.-H. L., Musacchio, M., & Lander, A. D. (2009) · Neural Development · doi:10.1186/1749-8104-4-33 · Cited by 128 · see citing works
Fjell, A. M., Westlye, L. T., Amlien, I. K., Tamnes, C. K., Grydeland, H., Engvig, A., Espeseth, T., Reinvang, I., Lundervold, A. J., Lundervold, A. J., et al. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht201 · Cited by 125 · see citing works
Griveau, A., Borello, U., Causeret, F., Tissir, F., Boggetto, N., Karaz, S., & Pierani, A. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000440 · Cited by 124 · see citing works
Identifying gene regulatory networks in schizophrenia
Potkin, S. G., Macciardi, F. M., Guffanti, G., Fallon, J. H., Wang, Q., Turner, J. A., Lakatos, A., Miles, M. F., Lander, A. D., Vawter, M. P., et al. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.06.036 · Cited by 112 · see citing works
FGF8 acts as a classic diffusible morphogen to pattern the neocortex
Toyoda, R., Assimacopoulos, S., Wilcoxon, J., Taylor, A., Feldman, P., Suzuki‐Hirano, A., Shimogori, T., & Grove, E. A. (2010) · Development · doi:10.1242/dev.055392 · Cited by 110 · see citing works
Fibroblast growth factor signaling in development of the cerebral cortex
Iwata, T., & Hevner, R. F. (2009) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2009.01104.x · Cited by 108 · see citing works
A Boolean Model of the Gene Regulatory Network Underlying Mammalian Cortical Area Development
Giacomantonio, C. E., & Goodhill, G. J. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000936 · Cited by 105 · see citing works
Nonomura, K., Yamaguchi, Y., Hamachi, M., Koike, M., Uchiyama, Y., Nakazato, K., Mochizuki, A., Sakaue-Sawano, A., Miyawaki, A., Yoshida, H., et al. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.11.015 · Cited by 103 · see citing works
Cortical neurogenesis and morphogens: diversity of cues, sources and functions
Tiberi, L., Vanderhaeghen, P., & van den Ameele, J. (2012) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2012.01.010 · Cited by 103 · see citing works
FGF signaling is strictly required to maintain early telencephalic precursor cell survival
Paek, H., Gutin, G., & Hébert, J. (2009) · Development · doi:10.1242/dev.032656 · Cited by 111 · see citing works
The cortical hem regulates the size and patterning of neocortex
Caronia, G., Yoshida, M., Gulden, F. O., Assimacopoulos, S., & Grove, E. A. (2014) · Development · doi:10.1242/dev.106914 · Cited by 96 · see citing works
Stevens, H. E. (2010) · Frontiers in Neuroscience · doi:10.3389/fnins.2010.00059 · Cited by 90 · see citing works
Berbel, P. J., Navarro, D., & Román, G. C. (2014) · Frontiers in Endocrinology · doi:10.3389/fendo.2014.00146 · Cited by 85 · see citing works
A Matter of Balance: Role of Neurexin and Neuroligin at the Synapse
Bang, M., & Owczarek, S. (2013) · Neurochemical Research · doi:10.1007/s11064-013-1029-9 · Cited by 86 · see citing works
Micali, N., Ma, S., Li, M., Kim, S., Mato-Blanco, X., Sindhu, S. K., Arellano, J. I., Gao, T., Shibata, M., Gobeske, K. T., et al. (2023) · Science · doi:10.1126/science.adf3786 · Cited by 82 · see citing works
Neocortical neurogenesis: morphogenetic gradients and beyond
Caviness, V. S., Nowakowski, R. S., & Bhide, P. G. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2009.05.003 · Cited by 78 · see citing works
Dysregulated fibroblast growth factor (FGF) signaling in neurological and psychiatric disorders
Turner, C. A., Eren‐Koçak, E., Inui, E. G., Watson, S. J., & Akil, H. (2015) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2015.10.003 · Cited by 75 · see citing works
Comparative mouse brain tractography of diffusion magnetic resonance imaging
Moldrich, R. X., Pannek, K., Hoch, R. V., Rubenstein, J. L. R., Kurniawan, N. D., & Richards, L. J. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.03.035 · Cited by 73 · see citing works
Self-citationShawa, H. E., Abbott, C. W., & Huffman, K. J. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3721-13.2013 · Cited by 72 · see citing works
Precision in the development of neocortical architecture: From progenitors to cortical networks
Kast, R. J., & Levitt, P. R. (2019) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2019.01.003 · Cited by 70 · see citing works
Lmo4 Establishes Rostral Motor Cortex Projection Neuron Subtype Diversity
Cederquist, G., Azim, E., Shnider, S. J., Padmanabhan, H. K., & Macklis, J. D. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.5140-12.2013 · Cited by 71 · see citing works
Emx2 and early hair cell development in the mouse inner ear
Holley, M. C., Rhodes, C. R., Kneebone, A., Herde, M. K., Fleming, M. T., & Steel, K. P. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2010.02.004 · Cited by 69 · see citing works
Velasquez, J. T., Watts, M. E., Todorovic, M., Nazareth, L., Pastrana, É., Díaz‐Nido, J., Lim, F., Ekberg, J. A. K., Quinn, R. J., & John, J. A. S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0111787 · Cited by 68 · see citing works
Saulnier, A., Keruzoré, M., Clercq, S. D., Bar, I., Moers, V., Magnani, D., Walcher, T., Filippis, C., Kricha, S., Parlier, D., et al. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs234 · Cited by 66 · see citing works
Pbx Regulates Patterning of the Cerebral Cortex in Progenitors and Postmitotic Neurons
Golonzhka, O., Nord, A. S., Tang, P. L.-F., Lindtner, S., Ypsilanti, A. R., Ferretti, E., Visel, A., Selleri, L., & Rubenstein, J. L. R. (2015) · Neuron · doi:10.1016/j.neuron.2015.10.045 · Cited by 66 · see citing works
Self-citationYpsilanti, A. R., & Rubenstein, J. L. R. (2015) · The Journal of Comparative Neurology · doi:10.1002/cne.23866 · Cited by 62 · see citing works
Self-citationThe evolution of the human brain and disease susceptibility
Pattabiraman, K., Muchnik, S. K., & Šestan, N. (2020) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2020.05.004 · Cited by 57 · see citing works
Postmitotic control of sensory area specification during neocortical development
Alfano, C., Magrinelli, E., Harb, K., Hevner, R. F., & Studer, M. (2014) · Nature Communications · doi:10.1038/ncomms6632 · Cited by 63 · see citing works
Molecular regulation of the developing commissural plate
Moldrich, R. X., Gobius, I., Pollak, T., Zhang, J., Ren, T., Brown, L. Y., Mori, S., Romero, C. D. J., Britanova, O. V., Tarabykin, V. S., et al. (2010) · The Journal of Comparative Neurology · doi:10.1002/cne.22445 · Cited by 61 · see citing works
Sp8 and COUP-TF1 Reciprocally Regulate Patterning and Fgf Signaling in Cortical Progenitors
Borello, U., Madhavan, M., Vilinsky, I., Faedo, A., Pierani, A., Rubenstein, J. L. R., & Campbell, K. (2013) · Cerebral Cortex · doi:10.1093/cercor/bhs412 · Cited by 59 · see citing works
Self-citationOchi, S., Manabe, S., Kikkawa, T., & Osumi, N. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23116115 · Cited by 58 · see citing works
Neocortical arealization: Evolution, mechanisms, and open questions
Alfano, C., & Studer, M. (2012) · Developmental Neurobiology · doi:10.1002/dneu.22067 · Cited by 57 · see citing works
Role of Fgf8 signalling in the specification of rostral Cajal-Retzius cells
Zimmer, C., Lee, J., Griveau, A., Arber, S., Pierani, A., Garel, S., & Guillemot, F. (2009) · Development · doi:10.1242/dev.041178 · Cited by 48 · see citing works
Fibroblast Growth Factor 8 Organizes the Neocortical Area Map and Regulates Sensory Map Topography
Assimacopoulos, S., Kao, T., Issa, N. P., & Grove, E. A. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0071-12.2012 · Cited by 47 · see citing works
Genetic Regulation of Vertebrate Forebrain Development by Homeobox Genes
Leung, R. F., George, A. M., Roussel, E., Faux, M. C., Wigle, J. T., & Eisenstat, D. D. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.843794 · Cited by 37 · see citing works
Quantification and Discrimination of Abnormal Sulcal Patterns in Polymicrogyria
Im, K., Pienaar, R., Paldino, M. J., Gaab, N., Galaburda, A. M., & Grant, P. E. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs292 · Cited by 43 · see citing works
Hoch, R. V., Clarke, J. A., & Rubenstein, J. L. R. (2015) · Neural Development · doi:10.1186/s13064-015-0037-7 · Cited by 40 · see citing works
Self-citationThe nuclear receptors COUP-TF: a long-lasting experience in forebrain assembly
Alfano, C., Magrinelli, E., Harb, K., & Studer, M. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1320-6 · Cited by 38 · see citing works
Molecular Regulation of Striatal Development: A Review
Evans, A. E., Kelly, C. M., Precious, S. V., & Rosser, A. (2012) · Anatomy Research International · doi:10.1155/2012/106529 · Cited by 40 · see citing works
Clercq, S. D., Keruzoré, M., Desmaris, E., Pollart, C., Assimacopoulos, S., Preillon, J., Ascenzo, S., Matson, C. K., Lee, M., Nan, X., et al. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw384 · Cited by 40 · see citing works
Fibroblast growth factor-2 regulation of sprouty and NR4A genes in bovine ovarian granulosa cells
Jiang, Z., Ripamonte, P., Junior, J. B., Portela, V. M., & Price, C. A. (2010) · Journal of Cellular Physiology · doi:10.1002/jcp.22509 · Cited by 39 · see citing works
Research models of neurodevelopmental disorders: The right model in the right place
Damianidou, E., Mouratidou, L., & Kyrousi, C. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.1031075 · Cited by 36 · see citing works
Charting the protomap of the human telencephalon
Clowry, G. J., Alzu’bi, A., Harkin, L. F., Sarma, S., Kerwin, J. M., & Lindsay, S. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.08.033 · Cited by 33 · see citing works
Huffman, K. J. (2012) · Frontiers in Genetics · doi:10.3389/fgene.2012.00212 · Cited by 35 · see citing works
Developmental Genes and Malformations in the Hypothalamus
Dı́az, C., & Puelles, L. (2020) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2020.607111 · Cited by 33 · see citing works
A histochemical study on condylar cartilage and glenoid fossa during mandibular advancement
Owtad, P., Potres, Z., Shen, G., Petocz, P., & Darendeliler, M. A. (2011) · The Angle Orthodontist · doi:10.2319/021710-99.1 · Cited by 35 · see citing works
Stimulating the proliferation, migration and lamellipodia of Schwann cells using low-dose curcumin
Velasquez, J. T., Nazareth, L., Quinn, R. J., Ekberg, J. A. K., & John, J. A. S. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.02.073 · Cited by 35 · see citing works
A Lifespan Analysis of Intraneocortical Connections and Gene Expression in the Mouse II
Dye, C. A., Shawa, H. E., & Huffman, K. J. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq213 · Cited by 33 · see citing works
Emergence of neuronal diversity from patterning of telencephalic progenitors
Azzarelli, R., Hardwick, L. J. A., & Philpott, A. (2015) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.174 · Cited by 30 · see citing works
Bilateral enucleation alters gene expression and intraneocortical connections in the mouse
Dye, C. A., Abbott, C. W., & Huffman, K. J. (2012) · Neural Development · doi:10.1186/1749-8104-7-5 · Cited by 27 · see citing works
A Lifespan Analysis of Intraneocortical Connections and Gene Expression in the Mouse I
Dye, C. A., Shawa, H. E., & Huffman, K. J. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq212 · Cited by 28 · see citing works
Fgfr3 regulates development of the caudal telencephalon
Moldrich, R. X., Mezzera, C., Holmes, W. M., Goda, S. A., Brookfield, S., Rankin, A. J., Barr, E., Kurniawan, N. D., Dewar, D., Richards, L. J., et al. (2011) · Developmental Dynamics · doi:10.1002/dvdy.22636 · Cited by 26 · see citing works
FGF8-mediated gene regulation affects regional identity in human cerebral organoids
Bertacchi, M., Maharaux, G., Loubat, A., Jung, M., & Studer, M. (2024) · eLife · doi:10.7554/elife.98096 · Cited by 20 · see citing works
Regulation and action of early growth response 1 in bovine granulosa cells
Han, P., Guerrero‐Netro, H. M., Estienne, A., Cao, B., & Price, C. A. (2017) · Reproduction · doi:10.1530/rep-17-0243 · Cited by 21 · see citing works
Differential requirements for Fgf3 and Fgf8 during mouse forebrain development
Theil, T., Domínguez‐Frutos, E., & Schimmang, T. (2008) · Developmental Dynamics · doi:10.1002/dvdy.21765 · Cited by 21 · see citing works
Chung, W. C. J., Linscott, M. L., Rodriguez, K. M., & Stewart, C. E. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00114 · Cited by 20 · see citing works
Scaling Proprioceptor Gene Transcription by Retrograde NT3 Signaling
Lee, J. H., Friese, A., Mielich, M., Sigrist, M., & Arber, S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045551 · Cited by 18 · see citing works
Wiring of higher-order cortical areas: Spatiotemporal development of cortical hierarchy
Teissier, A., & Pierani, A. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.05.010 · Cited by 17 · see citing works
Map transfer from the thalamus to the neocortex: Inputs from the barrel field
Lokmane, L., & Garel, S. (2014) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2014.07.005 · Cited by 18 · see citing works
Collette, J. C., Choubey, L., & Smith, K. M. (2017) · PeerJ · doi:10.7717/peerj.3519 · Cited by 18 · see citing works
Hang, C. Y., Kitahashi, T., & Parhar, I. S. (2014) · The Journal of Comparative Neurology · doi:10.1002/cne.23645 · Cited by 18 · see citing works
Direct Interactions BetweenGli3,Wnt8b, andFgfsUnderlie Patterning of the Dorsal Telencephalon
Hasenpusch‐Theil, K., Watson, J. A., & Theil, T. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv291 · Cited by 17 · see citing works
Punetha, M., Chouhan, V. S., Sonwane, A., Singh, G., Bag, S., Green, J. A., Whitworth, K. M., & Sarkar, M. (2020) · Scientific Reports · doi:10.1038/s41598-020-63804-z · Cited by 18 · see citing works
The Principle of Cortical Development and Evolution
Yang, Z. (2024) · Neuroscience Bulletin · doi:10.1007/s12264-024-01259-2 · Cited by 18 · see citing works
Torii, M., RAKIC, P. T., & Levitt, P. R. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23195 · Cited by 17 · see citing works
A role for sustained MAPK activity in the mouse ventral telencephalon
Talley, M. J., Nardini, D., Qin, S., Prada, C. E., Ehrman, L. A., & Waclaw, R. R. (2021) · Developmental Biology · doi:10.1016/j.ydbio.2021.03.019 · Cited by 17 · see citing works
ERK signaling expands mammalian cortical radial glial cells and extends the neurogenic period
Sun, M., Gao, Y., Li, Z., Yang, L., Liu, G., Xu, Z., Guo, R., You, Y., & Yang, Z. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2314802121 · Cited by 18 · see citing works
Yu, X., Nieman, B. J., Sudarov, A., Szulc, K. U., Abdollahian, D. J., Bhatia, N., Lalwani, A. K., Joyner, A. L., & Turnbull, D. H. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.02.068 · Cited by 16 · see citing works
Morphogens, Patterning Centers, and their Mechanisms of Action
Grove, E. A., & Monuki, E. S. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-397265-1.00019-8 · Cited by 16 · see citing works
Neurogenesis in the Basal Ganglia
Rubenstein, J. L. R., & Campbell, K. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-397265-1.00097-6 · Cited by 14 · see citing works
Self-citationTaguchi, Y. (2013) · BioData Mining · doi:10.1186/1756-0381-6-11 · Cited by 15 · see citing works
Shaydurov, V. A., Kasianov, A. S., & Bolshakov, A. P. (2018) · Journal of Molecular Neuroscience · doi:10.1007/s12031-018-1037-y · Cited by 14 · see citing works
Hryciw, T., MacDonald, J. I., Phillips, R., Seah, C., Pasternak, S., & Meakin, S. O. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06503.x · Cited by 12 · see citing works
Genetic Effects on Fine-Grained Human Cortical Regionalization
Cui, Y. J., Liu, B., Zhou, Y., Fan, L., Li, J., Zhang, Y., Wu, H., Hou, B., Wang, C., Zheng, F., et al. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv176 · Cited by 12 · see citing works
Genetic Resolutions of Brain Convolutions
Rash, B. G., & RAKIC, P. T. (2014) · Science · doi:10.1126/science.1250246 · Cited by 12 · see citing works
Neuroscience and Human Brain Evolution
Reyes, L. D., & Sherwood, C. C. (2014) · Springer series in bio-/neuroinformatics · doi:10.1007/978-3-319-08500-5_2 · Cited by 12 · see citing works
McMurtrey, R. J. (2016) · Journal of Tissue Engineering · doi:10.1177/2041731416671926 · Cited by 13 · see citing works
Martínez‐Frías, M. L., Egüés, X., Puras, A., Hualde, J. B., de Frutos, C. A., Bermejo, E., Nieto, M. A., & Martı́nez, S. (2010) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.33765 · Cited by 11 · see citing works
Molecular bases of cortico-cerebral regionalization
Mallamaci, A. (2011) · Progress in brain research · doi:10.1016/b978-0-444-53884-0.00017-8 · Cited by 10 · see citing works
Development and Developmental Disorders of the Cerebral Cortex
ten Donkelaar, H. J., Lammens, M. M. Y., Aronica, E., van Bokhoven, H., Ulzen, K. K.-V., & Hori, A. (2014) · Springer eBooks · doi:10.1007/978-3-642-54687-7_10 · Cited by 9 · see citing works
Clegg, J. M., Parkin, H. M., Mason, J. O., & Pratt, T. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1747-17.2018 · Cited by 9 · see citing works
Jones, W. D., Guadiana, S. M., & Grove, E. A. (2019) · The Journal of Comparative Neurology · doi:10.1002/cne.24643 · Cited by 9 · see citing works
- Authors
- Cholfin, J. A., & Rubenstein, J. L. R.
- Affiliations
- University of California, San Francisco (US)
- Corresponding author
- Rubenstein, John L.R.
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 2008-05-05
- Volume
- 509
- Issue
- 2
- Pages
- 144-155
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- PMC
- PMC4399554
- OpenAlex
- W2046996481
- Cited by
- 137
- References
- 60
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 6 · 2023: 3 · 2022: 4 · 2021: 5 · 2020: 7 · 2019: 7 · 2018: 1 · 2017: 5 · 2016: 8 · 2015: 7 · 2014: 11 · 2013: 14 · 2012: 12
- FWCI
- 3.87
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (K05MH065670)
- National Institute of Neurological Disorders and Stroke (R01NS034661, NS34661-01A1)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fibroblast Growth Factor Research
- Keywords
- frontal cortex, FGF8, FGF17, Emx2, fibroblast growth factor, SPRY1, SPRY2, ER81, ERM, PEA3, Sp8, transcription factors, gene expression biomarkers, double mutants, mouse brain development
- MeSH terms
- Empty Spiracles Homeobox Proteins, Amino Acid Sequence, Animals, Animals, Newborn, Fibroblast Growth Factors, Frontal Lobe, Mice, Inbred C57BL, Models, Neurological, Molecular Sequence Data, Morphogenesis, Nerve Tissue Proteins, Organ Specificity, Transcription Factors, Transcription, Genetic, Signal Transduction, Mice, Knockout, Homeodomain Proteins, Gene Expression Regulation, Developmental, Neuroepithelial Cells, Mice, Fibroblast Growth Factor 8, Forkhead Transcription Factors
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review