Renshaw cell interneuron specialization is controlled by a temporally restricted transcription factor program
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The spinal cord contains a diverse array of physiologically distinct interneuron cell types that subserve specialized roles in somatosensory perception and motor control. The mechanisms that generate these specialized interneuronal cell types from multipotential spinal progenitors are not known. In this study, we describe a temporally regulated transcriptional program that controls the differentiation of Renshaw cells (RCs), an anatomically and functionally discrete spinal interneuron subtype. We show that the selective activation of the Onecut transcription factors Oc1 and Oc2 during the first wave of V1 interneuron neurogenesis is a key step in the RC differentiation program. The development of RCs is additionally dependent on the forkhead transcription factor Foxd3, which is more broadly expressed in postmitotic V1 interneurons. Our demonstration that RCs are born, and activate Oc1 and Oc2 expression, in a narrow temporal window leads us to posit that neuronal diversity in the developing spinal cord is established by the composite actions of early spatial and temporal determinants.
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Onecut TFs have been shown to be expressed early in V1 and MNs.
“onecut TFs have been shown to be expressed early in V1 and MNs (Roy et al., 2012; Stam et al., 2012)”
From Single cell transcriptomics reveals spatial and temporal dynamics of gene expression in the developing mouse spinal cord (2019) · cites this paper as Stam et al., 2012
The onset of expression of Sox9 coincides with the switch of V1 neurons from Renshaw cells (onecut-expressing) to Foxp2-expressing neurons.
“The onset of expression of Sox9 coincides with the switch of V1 neurons from Renshaw cells (onecut-expressing) to Foxp2-expressing neurons (Kang et al., 2012; Stam et al., 2012; Stolt et al., 2003).”
From Single cell transcriptomics reveals spatial and temporal dynamics of gene expression in the developing mouse spinal cord (2019) · cites this paper as Stam et al., 2012
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BackgroundOgura, T., Sakaguchi, H., Miyamoto, S., & Takahashi, J. (2018) · Development · doi:10.1242/dev.162214 · Cited by 183 · see citing works
Britz, O., Zhang, J., Grossmann, K. S., Dyck, J. R. B., Kim, J. C., Dymecki, S. M., Gosgnach, S., & Goulding, M. (2015) · eLife · doi:10.7554/elife.04718 · Cited by 139 · see citing works
“When a R26 ds-HTB reporter mouse ( Stam et al., 2012 ) was used to assess the extent of En1 Cre and Cdx2-FlpO recombination in V1 INs, GFP reporter expression was activated in virtually all V1-derived cells at lumbosacral levels ( Figure 1E,F ).”
MethodMenelaou, E., & McLean, D. L. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.1809-12.2012 · Cited by 116 · see citing works
“Timing of development has also recently been implicated in the functional specification of limb motor networks (Tripodi et al., 2011; Benito-Gonzalez and Alvarez, 2012; Stam et al., 2012).”
BackgroundA shared transcriptional code orchestrates temporal patterning of the central nervous system
Sagner, A., Zhang, I., Watson, T., Lázaro, J., Melchionda, M., & Briscoe, J. (2021) · PLoS Biology · doi:10.1371/journal.pbio.3001450 · Cited by 128 · see citing works
“Onecut TFs, for example, are required in early-born V1 and MNs for the specification of Renshaw cells and medial lateral motor column (LMCm) neurons, respectively [31,36].”
BackgroundOrigin and segmental diversity of spinal inhibitory interneurons
Sweeney, L. B., Bikoff, J. B., Gabitto, M. I., Brenner-Morton, S., Baek, M., Yang, J. H., Tabak, E. G., Dasen, J. S., Kintner, C. R., & Jessell, T. M. (2018) · Neuron · doi:10.1016/j.neuron.2017.12.029 · Cited by 116 · see citing works
“Interestingly, the transcriptional profile of one of these candidate cell types, V1MafA+MafB+Oc2+Zfhx4+Oc1, mirrors that of a Renshaw cell (Stam et al., 2012), which is known to exist at all spinal cord levels (Benito-Gonzalez and Alvarez, 2012; Kirkwood et al., 1981).”
InfluentialAhmed, M. I., Alam, M. A., Emelianov, V. U., Poterlowicz, K., Patel, A., Sharov, A. A., Mardaryev, A. N., & Botchkareva, N. V. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201404001 · Cited by 120 · see citing works
RORβ Spinal Interneurons Gate Sensory Transmission during Locomotion to Secure a Fluid Walking Gait
Koch, S. C., Del Barrio, M. G., Dalet, A., Gatto, G., Günther, T., Zhang, J., Seidler, B., Saur, D., Schüle, R., & Goulding, M. (2017) · Neuron · doi:10.1016/j.neuron.2017.11.011 · Cited by 102 · see citing works
Self-citationFunctional subpopulations of V3 interneurons in the mature mouse spinal cord
Borowska, J., Jones, C. T., Zhang, H., Blacklaws, J., Goulding, M., & Zhang, Y. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.2005-13.2013 · Cited by 111 · see citing works
“For example, Renshaw cells, a subset of the V1 INs (Stam et al., 2012; Alvarez et al., 2013), mediate the recurrent inhibition to motor neurons and have unique anatomical and physiological characteristics (Renshaw, Received April 30, 2013; revised Oct. 11, 2013; accepted Oct. 23, 2013.”
BackgroundSelf-citationVillaescusa, J. C., Li, B., Toledo, E. M., Cervo, P. R. D. V., Yang, S., Stott, S., Kaiser, K., Islam, S., Gyllborg, D., Laguna‐Goya, R., et al. (2016) · The EMBO Journal · doi:10.15252/embj.201593725 · Cited by 109 · see citing works
A Functional Topographic Map for Spinal Sensorimotor Reflexes
Gatto, G., Bourane, S., Ren, X., Di Costanzo, S., Fenton, P. K., Halder, P., Seal, R. P., & Goulding, M. D. (2021) · Neuron · doi:10.1016/j.neuron.2020.10.003 · Cited by 92 · see citing works
“Rabies Virus Tracing—Focal injections of EnvA-pseudotyped, SADB19-ΔG-mCherry rabies virus (each of 250 nl; ~3.3×1010 units per ml) were made bilaterally in the lumbar (L2-L4 segments) dorsal horn of P4-P10 mice expressing the R26ds-HTB allele in homozygosity in combination with the described Cre/FlpO alleles.”
InfluentialSelf-citationFrancius, C., Harris, A., Rucchin, V., Hendricks, T. J., Stam, F. J., Barber, M., Kurek, D., Grosveld, F. G., Pierani, A., Goulding, M., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0070325 · Cited by 97 · see citing works
“While recent studies have described the expression of several transcriptional regulators in the developing spinal cord, including BhlhB5 [53] or Prdm8 [54], the Cut homeobox transcription factors of Onecut family such as HNF-6, OC-2 and OC-3 [55] and the bZIP transcription factors MafA, MafB [44] and cMaf, the relatio…”
BackgroundResultInfluentialDelineating the Diversity of Spinal Interneurons in Locomotor Circuits
Gosgnach, S., Bikoff, J. B., Dougherty, K. J., Manira, A. E., Lanuza, G. M., & Zhang, Y. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1829-17.2017 · Cited by 100 · see citing works
“As locomotor speed increases, the excitatory V0V cells are recruited to regulate contralateral motor output and activate last-order inhibitory interneurons located close to their target motoneurons (Talpalar et al., 2013).”
BackgroundThe late and dual origin of cerebrospinal fluid-contacting neurons in the mouse spinal cord
Petracca, Y. L., Sartoretti, M. M., Di Bella, D. J., Marin-Burgin, A., Carcagno, A. L., Schinder, A. F., & Lanuza, G. M. (2016) · Development · doi:10.1242/dev.129254 · Cited by 90 · see citing works
“Although other cases have been reported in which the temporal component contributes to neuronal diversity in the spinal cord (Gross et al., 2002; Stam et al., 2012), we provide robust evidence of neuronal differentiation occurring in what has been classically termed the gliogenic phase, proving that neurogenic potenti…”
BackgroundCell type and circuit modules in the spinal cord
Osseward, P. J., & Pfaff, S. L. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2019.03.003 · Cited by 87 · see citing works
Bayesian sparse regression analysis documents the diversity of spinal inhibitory interneurons
Gabitto, M. I., Pakman, A., Bikoff, J. B., Abbott, L. F., Jessell, T. M., & Paninski, L. (2016) · Cell · doi:10.1016/j.cell.2016.01.026 · Cited by 73 · see citing works
Peeling back the layers of locomotor control in the spinal cord
McLean, D. L., & Dougherty, K. J. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.03.001 · Cited by 78 · see citing works
Roy, A., Francius, C., Rousso, D. L., Seuntjens, E., Debruyn, J., Luxenhofer, G., Huber, A. B., Huylebroeck, D., Novitch, B. G., & Clotman, F. (2012) · Development · doi:10.1242/dev.078501 · Cited by 75 · see citing works
“…2003b; Vanhorenbeeck et al., 2007), where they regulate the generation, maintenance or the projections of different encephalic structures (Hodge et al., 2007; Chakrabarty et al., 2012; Espana and Clotman, 2012a; Espana and Clotman, 2012b) and of a spinal interneuron population (Stam et al., 2012).”
BackgroundBarrio, M. G. D., Bourane, S., Grossmann, K. S., Schüle, R., Britsch, S., O’Leary, D. D. M., & Goulding, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077928 · Cited by 65 · see citing works
“This is probably due to the loss of an enhancer element in the MafB-GFP knock-in allele that directs GFP expression in excitatory neurons [22,32].”
BackgroundSingle-cell transcriptomic analysis reveals diversity within mammalian spinal motor neurons
Liau, E. S., Jin, S., Chen, Y., Liu, W., Yong, L. W., Tsai, C.-T., Calon, M., Yu, J., Su, Y.-H., Nedelec, S., et al. (2023) · Nature Communications · doi:10.1038/s41467-022-35574-x · Cited by 60 · see citing works
Inhibition downunder: an update from the spinal cord
Goulding, M., Bourane, S., García‐Campmany, L., Dalet, A., & Koch, S. C. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.03.006 · Cited by 55 · see citing works
“During development, the V1 interneuron population displays a strict temporal program of that segregates Renshaw cell neurogenesis from the development of other V1 neuron cell types [55 ,56 ].”
BackgroundDirect Neuronal Differentiation of Neural Stem Cells for Spinal Cord Injury Repair
Xue, W., Fan, C., Chen, B., Zhao, Y., Xiao, Z., & Dai, J. (2021) · Stem Cells · doi:10.1002/stem.3366 · Cited by 55 · see citing works
Tozaki‐Saitoh, H., Masuda, J., Kawada, R., Kojima, C., Yoneda, S., Masuda, T., Inoue, K., & Tsuda, M. (2019) · Glia · doi:10.1002/glia.23570 · Cited by 52 · see citing works
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Evolution of mammalian sound localization circuits: A developmental perspective
Nothwang, H. G. (2016) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2016.02.003 · Cited by 48 · see citing works
Klimova, L., Antosova, B., Kuzelova, A., Strnad, H., & Kozmík, Z. (2015) · Developmental Biology · doi:10.1016/j.ydbio.2015.02.023 · Cited by 47 · see citing works
Central and peripheral innervation patterns of defined axial motor units in larval zebrafish
Bello‐Rojas, S., Istrate, A. E., Kishore, S., & McLean, D. L. (2019) · The Journal of Comparative Neurology · doi:10.1002/cne.24689 · Cited by 46 · see citing works
Onecut transcription factors in development and disease.
Kropp, P. A., & GANNON, M. A. (2016) · PubMed · Cited by 43 · see citing works
Espana, A., & Clotman, F. (2012) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2012.04.002 · Cited by 42 · see citing works
“In the CNS, the expression of the OC factors has been reported in the spinal cord where they are dynamically and differentially expressed in motor neurons and in subsets of ventral interneurons (Francius and Clotman, 2010; Stam et al., 2012), in different cell types in retina (Wu et al.”
BackgroundRegulation of motor circuit assembly by spatial and temporal mechanisms
Tripodi, M., & Arber, S. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.02.011 · Cited by 39 · see citing works
Wreden, C. C., Meng, J. L., Feng, W., Chi, W., Marshall, Z. D., & Heckscher, E. S. (2017) · Current Biology · doi:10.1016/j.cub.2017.04.024 · Cited by 37 · see citing works
“For example, Renshaw cells and Ia interneurons are sequentially produced by p1 progenitors [27, 28].”
BackgroundGABAergic Neuron Specification in the Spinal Cord, the Cerebellum, and the Cochlear Nucleus
Hori, K., & Hoshino, M. (2012) · Neural Plasticity · doi:10.1155/2012/921732 · Cited by 36 · see citing works
“The V1 interneurons are initially generated as a homogeneous GABAergic interneuron population in developing neural tubes [51] but subsequently differentiate into a range of inhibitory interneuron cell types, including Renshaw cells (RCs) and putative reciprocal Ia inhibitory interneurons [52, 54, 55].”
BackgroundKabayiza, K. U., Masgutova, G., Harris, A., Rucchin, V., Jacob, B., & Clotman, F. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00157 · Cited by 35 · see citing works
“As previously reported in motor neurons and ventral interneurons (Francius and Clotman, 2010; Stam et al., 2012; Francius et al., 2013), the distribution of the three Onecut proteins in dINs was partially overlapping.”
BackgroundInfluentialIntegration of Spatial and Temporal Patterning in the Invertebrate and Vertebrate Nervous System
Chen, Y., & Konstantinides, N. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.854422 · Cited by 35 · see citing works
Spinal cords: Symphonies of interneurons across species
Wilson, A. C., & Sweeney, L. B. (2023) · Frontiers in Neural Circuits · doi:10.3389/fncir.2023.1146449 · Cited by 36 · see citing works
“In mice, the V1 class includes the well-studied Renshaw cells and reciprocal Ia-interneuron subtypes which are believed to play a role in flexor-extensor inhibition (Eccles et al., 1956; Feldman and Orlovsky, 1975; Sapir et al., 2004; Alvarez et al., 2005; Benito-Gonzalez and Alvarez, 2012; Stam et al., 2012; Zhang et…”
BackgroundDeska‐Gauthier, D., Borowska-Fielding, J., Jones, C. T., & Zhang, Y. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1518-19.2019 · Cited by 33 · see citing works
“…to play crucial roles in the formation of dorsal Lbx1 INs (John et al., 2005); V0 INs (Satou et al., 2012); V1 Renshaw cells (Benito-Gonzalez and Alvarez, 2012; Stam et al., 2012); and most recently, Gata2/3 CSFcontacting neurons (CSF-cNs; Petracca et al., 2016) and V2a INs (Hayashi et al., 2018).”
BackgroundHarris, A., Masgutova, G., Collin, A. M., Toch, M., Hidalgo‐Figueroa, M., Jacob, B., Corcoran, L. M., Francius, C., & Clotman, F. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00184 · Cited by 31 · see citing works
Ascl1 Balances Neuronal versus Ependymal Fate in the Spinal Cord Central Canal.
Bella, D. J. D., Carcagno, A. L., Bartolomeu, M., Pardi, M. B., Löhr, H., Siegel, N., Hammerschmidt, M., Marin-Burgin, A., & Lanuza, G. M. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.07.087 · Cited by 19 · see citing works
Subtype diversification and synaptic specificity of stem cell-derived spinal interneurons
Hoang, P. T., Chalif, J. I., Bikoff, J. B., Jessell, T. M., Mentis, G. Z., & Wichterle, H. (2018) · Neuron · doi:10.1016/j.neuron.2018.09.016 · Cited by 25 · see citing works
From signalling to form: the coordination of neural tube patterning
Frith, T. J. R., Briscoe, J., & Boezio, G. L. M. (2023) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2023.11.004 · Cited by 31 · see citing works
Audouard, E., Schakman, O., René, F., Huettl, R.-E., Huber, A. B., Loeffler, J., Gailly, P. L., & Clotman, F. (2012) · PLoS ONE · doi:10.1371/journal.pone.0050509 · Cited by 31 · see citing works
“Furthermore, they regulate neuronal identity, migration, maintenance or projections in different regions of the CNS [23,24,25,26,27] Onecut factors are present in MN from the onset of their differentiation until birth [28].”
BackgroundHow prolonged expression of Hunchback, a temporal transcription factor, re-wires locomotor circuits
Meng, J. L., Marshall, Z. D., Lobb-Rabe, M., & Heckscher, E. S. (2019) · eLife · doi:10.7554/elife.46089 · Cited by 29 · see citing works
The functional diversity of spinal interneurons and locomotor control
Deska‐Gauthier, D., & Zhang, Y. (2019) · Current Opinion in Physiology · doi:10.1016/j.cophys.2019.01.005 · Cited by 28 · see citing works
Generating neural diversity through spatial and temporal patterning
Sen, S. (2022) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2022.06.002 · Cited by 28 · see citing works
A Role for Dystonia-Associated Genes in Spinal GABAergic Interneuron Circuitry
Zhang, J., Weinrich, J. A. P., Russ, J. B., Comer, J., Bommareddy, P., Dicasoli, R., Wright, C., Li, Y.-Q., van Roessel, P. J., & Kaltschmidt, J. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.09.079 · Cited by 25 · see citing works
“As such, our work supports and extends previous findings showing that multiple aspects of neuronal fate, including migratory behavior and ultimate cell body positioning, are associated with timing of neurogenesis (Tripodi et al., 2011; Benito-Gonzalez and Alvarez, 2012; Stam et al., 2012; Tripodi and Arber, 2012).”
ResultMeng, J. L., & Heckscher, E. S. (2020) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2020.11.010 · Cited by 24 · see citing works
Toch, M., Harris, A., Schakman, O., Kondratskaya, E., Boulland, J., Dauguet, N., Debrulle, S., Baudouin, C., Hidalgo‐Figueroa, M., Mu, X., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-57945-4 · Cited by 22 · see citing works
Embryonic temporal-spatial delineation of excitatory spinal V3 interneuron diversity
Deska‐Gauthier, D., Borowska-Fielding, J., Jones, C., Zhang, H., Mackay, C., Michail, R., Bennett, L. A., Bikoff, J. B., & Zhang, Y. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113635 · Cited by 21 · see citing works
“These findings aligned with previous work identifying RCs as the first V1 IN subpopulation to exit from the p1 progenitor domain before migrating ventrolaterally and forming a recurrent inhibitory feedback loop with motor neurons 34,35 .”
Boeri, J., Corronc, H. L., Lejeune, F., Bras, B. L., Mouffle, C., Angelim, M. K. S. C., Mangin, J., Branchereau, P., Legendre, P., & Czarnecki, A. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.3203-17.2018 · Cited by 21 · see citing works
Transcriptional and epigenetic regulation of temporal patterning in neural progenitors
Ray, A., Zhu, H., Ding, A. Z., & Li, X. (2021) · Developmental Biology · doi:10.1016/j.ydbio.2021.10.006 · Cited by 19 · see citing works
Audouard, E., Schakman, O., Ginion, A., Bertrand, L., Gailly, P. L., & Clotman, F. (2013) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2013.05.001 · Cited by 19 · see citing works
Francius, C., Hidalgo‐Figueroa, M., Debrulle, S., Pelosi, B., Rucchin, V., Ronellenfitch, K., Panayiotou, E., Makrides, N., Misra, K., Harris, A., et al. (2016) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2016.00145 · Cited by 18 · see citing works
“A′′′; Stam et al., 2012).”
BackgroundInfluentialPou2f2 Regulates the Distribution of Dorsal Interneurons in the Mouse Developing Spinal Cord
Masgutova, G., Harris, A., Jacob, B., Corcoran, L. M., & Clotman, F. (2019) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2019.00263 · Cited by 18 · see citing works
“, 2017) or maintenance (Espana and Clotman, 2012a,b; Stam et al., 2012) of specific neuronal populations, they also regulate neuronal distribution of various neuron types.”
BackgroundTemporal patterning of the vertebrate developing neural tube
Sagner, A. (2024) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2024.102179 · Cited by 17 · see citing works
Interneuron diversity and function in the spinal motor system
Bikoff, J. B. (2019) · Current Opinion in Physiology · doi:10.1016/j.cophys.2018.12.013 · Cited by 17 · see citing works
Lane, A. R., Cogdell, I. C., Jessell, T. M., Bikoff, J. B., & Álvarez, F. J. (2021) · Scientific Reports · doi:10.1038/s41598-021-99333-6 · Cited by 15 · see citing works
Hilscher, M. M., Mikulovic, S., Perry, S. E., Lundberg, S., & Kullander, K. (2023) · Pharmacological Research · doi:10.1016/j.phrs.2023.106895 · Cited by 15 · see citing works
“Calb1 , under the control of the transcription factors forkhead box D3 ( Foxd3 ) and MAF bZIP transcription factor B ( Mafb ), is upregulated soon after Renshaw cells begin differentiation and is retained in mature Renshaw cells but down-regulated in other early V1 populations [155,161,162].”
Seroka, A. Q., Yazejian, R. M., Lai, S.-L., & Doe, C. Q. (2020) · Neural Development · doi:10.1186/s13064-020-00146-6 · Cited by 14 · see citing works
CUT homeobox genes: transcriptional regulation of neuronal specification and beyond
Leyva‐Díaz, E. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1233830 · Cited by 14 · see citing works
“These defects include motor neuron atrophy, defects in neuromuscular junctions and in the formation of Renshaw cell interneurons, as well as faulty reorganization of cerebellar Purkinje cells (Audouard et al., 2012; Stam et al., 2012).”
BackgroundToch, M., & Clotman, F. (2019) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2019.103411 · Cited by 13 · see citing works
Mapping Connectivity Amongst Interneuronal Components of the Locomotor CPG
Haque, F., & Gosgnach, S. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00443 · Cited by 12 · see citing works
Lowenstein, E. D., Misios, A., Buchert, S., & Ruffault, P.-L. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.1441-23.2024 · Cited by 11 · see citing works
Timing neural development and regeneration
Blackshaw, S., & Cayouette, M. (2025) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2025.102976 · Cited by 11 · see citing works
The Temporal Mechanisms Guiding Interneuron Differentiation in the Spinal Cord
Deska‐Gauthier, D., & Zhang, Y. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22158025 · Cited by 11 · see citing works
The organization of spinal neurons: Insights from single cell sequencing
Roome, R. B., & Levine, A. J. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102762 · Cited by 11 · see citing works
“Moreover, the V1 and dI6 cardinal classes have also been shown to include neuron subtypes of different birthdates [25,50].”
BackgroundWorthy, A. E., Anderson, J. T., Lane, A. R., Gomez-Perez, L. J., Wang, A. A., Griffith, R. W., Rivard, A. F., Bikoff, J. B., & Álvarez, F. J. (2024) · eLife · doi:10.7554/elife.95172.3 · Cited by 10 · see citing works
Trevisan, A. J., Han, K., Chapman, P., Kulkarni, A. S., Hinton, J. M., Ramirez, C., Klein, I., Gatto, G., Gabitto, M. I., Menon, V., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.09.18.613279 · Cited by 9 · see citing works
Boeri, J., Meunier, C., Corronc, H. L., Branchereau, P., Timofeeva, Y., Lejeune, F., Mouffle, C., Arulkandarajah, K. H., Mangin, J., Legendre, P., et al. (2021) · eLife · doi:10.7554/elife.62639 · Cited by 7 · see citing works
Vassalli, Q. A., Colantuono, C., Nittoli, V., Ferraioli, A., Fasano, G., Berruto, F., Chiusano, M. L., Kelsh, R. N., Sordino, P., & Locascio, A. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.602450 · Cited by 7 · see citing works
Worthy, A. E., Anderson, J. T., Lane, A. R., Gomez-Perez, L. J., Wang, A. A., Griffith, R. W., Rivard, A. F., Bikoff, J. B., & Álvarez, F. J. (2024) · eLife · doi:10.7554/elife.95172 · Cited by 6 · see citing works
Espinosa, F., Pop, I. V., & Lai, H. C. (2024) · eNeuro · doi:10.1523/eneuro.0331-23.2024 · Cited by 5 · see citing works
“…Hippenmeyer et al., 2005), Hoxa4::Cre (Huang et al., 2012), R26 LSL-ChR2(H134R)-EYFP (Ai32; Madisen et al., 2012), R26 doublestop(ds)-HTB mouse (Stam et al., 2012; Li et al., 2013), RCE::RFrt (Miyoshi et al., 2010), R26 FSF-tdTom (Ai65 crossed to germline CRE recombinase to make a…”
Vijatovic, D., Toma, F. A., Harrington, Z. P. M., Sommer, C., Hauschild, R., Trevisan, A. J., Chapman, P., Julseth, M. J., Brenner‐Morton, S., Gabitto, M. I., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.09.20.614050 · Cited by 6 · see citing works
Multifold increase in spinal inhibitory cell types with emergence of limb movement
Vijatovic, D., Toma, F. A., Ignatyev, Y., Harrington, Z. P. M., Sommer, C., Hauschild, R., Smits, M., Vecchia, M. D., Trevisan, A. J., Chapman, P., et al. (2026) · Cell Reports · doi:10.1016/j.celrep.2026.117227 · Cited by 5 · see citing works
“Foxd3 , an independent marker of V1 inhibitory neurons, 71,75 was maintained in both wild-type and En1 mutant animals (Figure S13I–S13R and S13T), indicating that V1s still developed in the absence of En1 (Figure S13S) and giving us a secondary method to identify them and evaluate V1 subtype…”
Zirnheld, A. L. (2015) · Journal of Aging Science · doi:10.4172/2329-8847.1000140 · Cited by 3 · see citing works
“For example, ONECUT2, expressed in several cell types including neurons, is involved in development and differentiation of motor and sensory neurons, as well as the development of several brain regions [7-11].”
BackgroundHarris, A., Masgutova, G., Collin, A., Toch, M., Hidalgo-Figueroa, M., Jacob, B., Corcoran, L. M., Francius, C., & Clotman, F. (2018) · doi:10.1101/413054 · Cited by 2 · see citing works
Temporal Control of Neural Progenitors: TGF-β Switches the Clock Forward
Mattar, P. A., & Cayouette, M. (2014) · Neuron · doi:10.1016/j.neuron.2014.11.013 · Cited by 3 · see citing works
“Moreover, recent reports 886 Neuron 84, December 3, 2014 ª2014 Els have hinted that in the prototypically spatial spinal cord some NPCs sequentially generate different neuron subtypes (Benito-Gonzalez and Alvarez, 2012; Stam et al., 2012).”
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Development and Developmental Disorders of the Spinal Cord
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Transcriptional regulators with broad expression in the zebrafish spinal cord
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“V1R constitute a homogeneous population in terms of their transcription factor program during development (Benito-Gonzalez & Alvarez 2012, Stam et al 2012), their physiological function (Eccles et al 1956) and their firing pattern at postnatal stages (Bikoff et al 2016).”
The Study of Sensorimotor Circuit Assembly in Drosophila melanogaster Embryos and LarvaePreprint
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“To do this, we used a mouse line that enables tracing synaptic inputs from starter cells that express both cre-and flp-recombinase (Rosa-DS-HTB) ( 63, 64 ).”
Petracca, Y. L. (2015) · Repositorio Digital Institucional de la Universidad de Buenos Aires (Universidad de Buenos Aires)
- Authors
- Stam, F. J., Hendricks, T. J., Zhang, J., Geiman, E. J., Francius, C., Labosky, P. A., Clotman, F., & Goulding, M.
- Affiliations
- Salk Institute for Biological Studies (US)
- Université Catholique de Louvain, Institute of Neuroscience, Laboratory of Neural Differentiation, Av. Hippocrate 55, B-1200 Brussels, Belgium.
- Vanderbilt University (US)
- Corresponding author
- Goulding, Martyn
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 2012-01-01
- Volume
- 139
- Issue
- 1
- Pages
- 179-190
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- PMC
- PMC3231776
- OpenAlex
- W2151506803
- Cited by
- 115
- References
- 77
- Citations by year
- 2026: 8 · 2025: 4 · 2024: 13 · 2023: 10 · 2022: 3 · 2021: 8 · 2020: 5 · 2019: 15 · 2018: 9 · 2017: 6 · 2016: 8 · 2015: 9 · 2014: 4 · 2013: 6 · 2012: 7
- FWCI
- 1.79
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Development (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Digital Access to Libraries (Université catholique de Louvain (UCL), l'Université de Namur (UNamur) and the Université Saint-Louis (USL-B)) (submittedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (R01NS037075, R37NS037075, NS037075)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD036720, HD036720)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Health Sciences › Medicine › Surgery › Congenital gastrointestinal and neural anomalies
- Keywords
- Renshaw cells, spinal interneurons, FOXD3, temporal gene regulation, neuronal differentiation, neuronal heterogeneity, spinal cord development, transcriptional programs
- MeSH terms
- Animals, Bromodeoxyuridine, Cell Differentiation, Crosses, Genetic, Electrophysiology, Immunohistochemistry, Interneurons, Spinal Cord, Time Factors, Transcription Factors, Homeodomain Proteins, Gene Expression Regulation, Developmental, Green Fluorescent Proteins, Mice, Hepatocyte Nuclear Factor 6
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