Dorsally derived spinal interneurons in locomotor circuits
Abstract
During neuronal circuit formation, axons are guided to their targets by the help of axon guidance molecules, which are required for establishing functional circuits. A promising system to dissect the development and functionalities of neuronal circuitry is the spinal cord central pattern generator (CPG) for locomotion, which converts a tonic supraspinal drive to rhythmic and coordinated movements. Here we describe concepts arising from genetic studies of the locomotor network with a focus on the position and roles of commissural interneurons. In particular, this involves studies of several families of axon guidance molecules relevant for midline crossing, the Eph/ephrins and Netrin/DCC. Effects on developing commissural interneurons in mice with aberrant midline axon guidance capabilities suggest that, in addition to ventral populations, dorsal commissural interneurons also play a role in coordinating locomotor circuitry. Recent findings implicate the novel dI6 interneuron marker Dmrt3 in this role. Strikingly, mutations in Dmrt3 result in divergent gait patterns in both mice and horses.
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A subset of cells from the dorsal dI4.6/dI6 lineages contributed to most ventral inhibitory populations.
“A subset of cells from the dorsal dI4.6/dI6 lineages contributed to most ventral inhibitory populations, which was unexpected though there have been reports of scattered dI4 Ptf1a-derived cells in the embryonic and perinatal ventral horn103,104, and the very small dI6 population is known to be ventrally located105–107.”
From A harmonized atlas of mouse spinal cord cell types and their spatial organization (2021) · cites this paper as [107]
Cites
Locomotion in vertebrates: central mechanisms and reflex interaction.
Grillner, S. (1975) · Physiological Reviews · doi:10.1152/physrev.1975.55.2.247 · Cited by 1,439 · see citing works
Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord
Kennedy, T. E., Serafini, T. A., de la Torre, J. R., & Tessier‐Lavigne, M. (1994) · Cell · doi:10.1016/0092-8674(94)90421-9 · Cited by 1,341 · see citing works
Netrin-1 Is Required for Commissural Axon Guidance in the Developing Vertebrate Nervous System
Serafini, T. A., Colamarino, S. A., Leonardo, E. D., Wang, H., Beddington, R. S. P., Skarnes, W. C., & Tessier‐Lavigne, M. (1996) · Cell · doi:10.1016/s0092-8674(00)81795-x · Cited by 1,286 · see citing works
A Developmental Switch in the Response of DRG Neurons to ETS Transcription Factor Signaling
Hippenmeyer, S., Pecho‐Vrieseling, E., Sigrist, M., Portmann, T., Laengle, C., Ladle, D. R., & Arber, S. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030159 · Cited by 1,059 · see citing works
Biological Pattern Generation: The Cellular and Computational Logic of Networks in Motion
Grillner, S. E. (2006) · Neuron · doi:10.1016/j.neuron.2006.11.008 · Cited by 920 · see citing works
Ericson, J., Brenner‐Morton, S., Kawakami, A., Roelink, H., & Jessell, T. M. (1996) · Cell · doi:10.1016/s0092-8674(00)81386-0 · Cited by 870 · see citing works
LOCOMOTOR CIRCUITS IN THE MAMMALIAN SPINAL CORD
Kiehn, O. (2006) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112910 · Cited by 868 · see citing works
The motor infrastructure: from ion channels to neuronal networks
Grillner, S. E. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1137 · Cited by 839 · see citing works
Homeobox gene Nkx2.2 and specification of neuronal identity by graded Sonic hedgehog signalling
Briscoe, J., Sussel, L., Serup, P., Hartigan-O'Connor, D., Jessell, T., Rubenstein, J., & Ericson, J. (1999) · Nature · doi:10.1038/19315 · Cited by 807 · see citing works
Circuits controlling vertebrate locomotion: moving in a new direction
Goulding, M. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2608 · Cited by 777 · see citing works
Organization of mammalian locomotor rhythm and pattern generation
McCrea, D. A., & Rybak, I. A. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.08.006 · Cited by 687 · see citing works
Common Principles of Motor Control in Vertebrates and Invertebrates
Pearson, K. G. (1993) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.16.030193.001405 · Cited by 567 · see citing works
Kjaerulff, O., & Kiehn, O. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-18-05777.1996 · Cited by 529 · see citing works
Lanuza, G. M., Gosgnach, S., Pierani, A., Jessell, T. M., & Goulding, M. (2004) · Neuron · doi:10.1016/s0896-6273(04)00249-1 · Cited by 450 · see citing works
Mutations in DMRT3 affect locomotion in horses and spinal circuit function in mice
Andersson, L. S., Larhammar, M., Memic, F., Wootz, H., Schwochow, D., Rubin, C., Patra, K., Árnason, T., Wellbring, L., Hjälm, G., et al. (2012) · Nature · doi:10.1038/nature11399 · Cited by 431 · see citing works
Self-citationA Cluster of Cholinergic Premotor Interneurons Modulates Mouse Locomotor Activity
Zagoraiou, L., Akay, T., Martin, J. F., Brownstone, R. M., Jessell, T. M., & Miles, G. B. (2009) · Neuron · doi:10.1016/j.neuron.2009.10.017 · Cited by 429 · see citing works
V1 spinal neurons regulate the speed of vertebrate locomotor outputs
Gosgnach, S., Lanuza, G. M., Butt, S. J. B., Saueressig, H., Zhang, Y., Velasquez, T., Riethmacher, D., Callaway, E. M., Kiehn, O., & Goulding, M. (2006) · Nature · doi:10.1038/nature04545 · Cited by 405 · see citing works
Jostes, B., Walther, C., & Gruß, P. (1990) · Mechanisms of Development · doi:10.1016/0925-4773(90)90132-6 · Cited by 400 · see citing works
Water Uptake, Diameter Change, and Nonlinear Diffusion in Tree Stems
Parlange, J., Turner, N. C., & Waggoner, P. E. (1975) · PLANT PHYSIOLOGY · doi:10.1104/pp.55.2.247 · Cited by 398 · see citing works
Lbx1 specifies somatosensory association interneurons in the dorsal spinal cord
Gross, M. K., Dottori, M., & Goulding, M. (2002) · Neuron · doi:10.1016/s0896-6273(02)00690-6 · Cited by 396 · see citing works
A topographic map of recruitment in spinal cord
McLean, D. L., Fan, J., Higashijima, S.-I., Hale, M. E., & Fetcho, J. R. (2007) · Nature · doi:10.1038/nature05588 · Cited by 384 · see citing works
Control of Interneuron Fate in the Developing Spinal Cord by the Progenitor Homeodomain Protein Dbx1
Pierani, A., Moran-Rivard, L., Sunshine, M. J., Littman, D. R., Goulding, M., & Jessell, T. M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00212-4 · Cited by 379 · see citing works
Müller, T., Brohmann, H., Pierani, A., Heppenstall, P. A., Lewin, G. R., Jessell, T. M., & Birchmeier, C. (2002) · Neuron · doi:10.1016/s0896-6273(02)00689-x · Cited by 368 · see citing works
Role of EphA4 and EphrinB3 in Local Neuronal Circuits That Control Walking
Kullander, K., Butt, S., Lebret, J. M., Lundfald, L., Restrepo, C. E., Rydström, A., Klein, R., & Kiehn, O. (2003) · Science · doi:10.1126/science.1079641 · Cited by 365 · see citing works
Self-citationCrone, S. A., Quinlan, K. A., Zagoraiou, L., Droho, S., Restrepo, C. E., Lundfald, L., Endo, T., Setlak, J., Jessell, T. M., Kiehn, O., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.08.009 · Cited by 358 · see citing works
V3 Spinal Neurons Establish a Robust and Balanced Locomotor Rhythm during Walking
Zhang, Y., Narayan, S., Geiman, E. J., Lanuza, G. M., Velasquez, T., Shanks, B., Akay, T., Dyck, J. R. B., Pearson, K. G., Gosgnach, S., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.027 · Cited by 350 · see citing works
SnapShot: spinal cord development
Alaynick, W. A., Jessell, T. M., & Pfaff, S. L. (2011) · Cell · doi:10.1016/j.cell.2011.06.038 · Cited by 338 · see citing works
Deletion of Ultraconserved Elements Yields Viable Mice
Ahituv, N., Zhu, Y., Visel, A., Holt, A., Afzal, V., Pennacchio, L. A., & Rubin, E. M. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050234 · Cited by 319 · see citing works
Proprioceptor Pathway Development Is Dependent on MATH1
Bermingham, N. A., Hassan, B. A., Wang, V. Y., Fernandez, M., Banfi, S., Bellen, H. J., Fritzsch, B., & Zoghbi, H. Y. (2001) · Neuron · doi:10.1016/s0896-6273(01)00305-1 · Cited by 304 · see citing works
Vallstedt, A., Muhr, J., Pattyn, A., Pierani, A., Mendelsohn, M., Sander, M., Jessell, T., & Ericson, J. (2001) · Neuron · doi:10.1016/s0896-6273(01)00412-3 · Cited by 288 · see citing works
Self-citationNeuron-glia communication via EphA4/ephrin-A3 modulates LTP through glial glutamate transport
Filosa, A., Paixão, S., Honsek, S. D., Carmona, M. A., Becker, L., Feddersen, B., Gaitanos, L., Rudhard, Y., Schoepfer, R., Klopstock, T., et al. (2009) · Nature Neuroscience · doi:10.1038/nn.2394 · Cited by 283 · see citing works
Self-citationProgenitors of dorsal commissural interneurons are defined by MATH1 expression
Helms, A. W., & Johnson, J. E. B. (1998) · Development · doi:10.1242/dev.125.5.919 · Cited by 279 · see citing works
Lamina VIII interneurones interposed in crossed reflex pathways in the cat.
Harrison, P. J., Jankowska, E., & Zytnicki, D. (1986) · The Journal of Physiology · doi:10.1113/jphysiol.1986.sp015965 · Cited by 266 · see citing works
In mice lacking V2a interneurons, gait depends on speed of locomotion
Crone, S. A., Zhong, G., Harris-Warrick, R., & Sharma, K. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1206-09.2009 · Cited by 263 · see citing works
Evx1 Is a Postmitotic Determinant of V0 Interneuron Identity in the Spinal Cord
Moran-Rivard, L., Kagawa, T., Saueressig, H., Gross, M. K., Burrill, J. D., & Goulding, M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00213-6 · Cited by 261 · see citing works
Kullander, K., Mather, N. K., Diella, F., Dottori, M., Boyd, A., & Klein, R. (2001) · Neuron · doi:10.1016/s0896-6273(01)00181-7 · Cited by 258 · see citing works
Self-citationStepien, A. E., Tripodi, M., & Arber, S. (2010) · Neuron · doi:10.1016/j.neuron.2010.10.019 · Cited by 246 · see citing works
Postnatal phenotype and localization of spinal cord V1 derived interneurons
Alvarez, F. J., Jonas, P. C., Sapir, T., Hartley, R., Berrocal, M. C., Geiman, E. J., Todd, A. J., & Goulding, M. (2005) · Journal of Comparative Neurology · doi:10.1002/cne.20711 · Cited by 243 · see citing works
Keller, C., Hansen, M. S., Coffin, C. M., & Capecchi, M. R. (2004) · Genes & Development · doi:10.1101/gad.1243904 · Cited by 235 · see citing works
Neuromodulation and flexibility in Central Pattern Generator networks
Harris‐Warrick, R. M. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.05.011 · Cited by 227 · see citing works
Stringent Specificity in the Construction of a GABAergic Presynaptic Inhibitory Circuit
Betley, J. N., Wright, C. V. E., Kawaguchi, Y., Erdélyi, F., Szabó, G., Jessell, T. M., & Kaltschmidt, J. A. (2009) · Cell · doi:10.1016/j.cell.2009.08.027 · Cited by 218 · see citing works
Burrill, J. D., Moran, L., Goulding, M., & Saueressig, H. (1997) · Development · doi:10.1242/dev.124.22.4493 · Cited by 210 · see citing works
Cowley, K. C., & Schmidt, B. J. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.74.3.1109 · Cited by 204 · see citing works
Motor antagonism exposed by spatial segregation and timing of neurogenesis
Tripodi, M., Stepien, A. E., & Arber, S. (2011) · Nature · doi:10.1038/nature10538 · Cited by 203 · see citing works
Wallén‐Mackenzie, Å., Gezelius, H., Thoby‐Brisson, M., Nygård, A., Enjin, A., Fujiyama, F., Fortin, G., & Kullander, K. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3855-06.2006 · Cited by 198 · see citing works
Self-citationPax6 and Engrailed 1 Regulate Two Distinct Aspects of Renshaw Cell Development
Sapir, T., Geiman, E. J., Wang, Z., Velasquez, T., Mitsui, S., Yoshihara, Y., Frank, E., Álvarez, F. J., & Goulding, M. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3187-03.2004 · Cited by 189 · see citing works
Saueressig, H., Burrill, J. D., & Goulding, M. (1999) · Development · doi:10.1242/dev.126.19.4201 · Cited by 188 · see citing works
Engrailed-1 Expression Marks a Primitive Class of Inhibitory Spinal Interneuron
Higashijima, S., Masino, M. A., Mandel, G., & Fetcho, J. R. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5342-03.2004 · Cited by 187 · see citing works
Strychnine eliminates alternating motor output during fictive locomotion in the lamprey.
Cohen, A., & Harris-Warrick, R. (1984) · Brain Research · doi:10.1016/0006-8993(84)91464-1 · Cited by 164 · see citing works
Brownstone, R. M., & Wilson, J. M. M. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.06.025 · Cited by 153 · see citing works
Sexually dimorphic expression of multiple doublesex-related genes in the embryonic mouse gonad
Kim, S., Kettlewell, J. R., Anderson, R. C., Bardwell, V. J., & Zarkower, D. A. (2003) · Gene Expression Patterns · doi:10.1016/s1567-133x(02)00071-6 · Cited by 137 · see citing works
The function of Dmrt genes in vertebrate development: It is not just about sex
Hong, C., Park, B., & Saint‐Jeannet, J. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.07.035 · Cited by 133 · see citing works
Segmental, Synaptic Actions of Commissural Interneurons in the Mouse Spinal Cord
Quinlan, K., & Kiehn, O. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1618-07.2007 · Cited by 132 · see citing works
Enjin, A., Bernhardt, N. R., Nakanishi, S. T., Vallstedt, A., Gezelius, H., Memic, F., Lind, M., Hjalt, T. Å. H., Tourtellotte, W. G., Bruder, C. E. G., et al. (2010) · The Journal of Comparative Neurology · doi:10.1002/cne.22332 · Cited by 130 · see citing works
Self-citationThe formation of sensorimotor circuits.
Goulding, M. D., Lanuza, G. M., Sapir, T., & Narayan, S. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00371-9 · Cited by 125 · see citing works
Primitive Roles for Inhibitory Interneurons in Developing Frog Spinal Cord
Li, W., Higashijima, S., Parry, D. M., Roberts, A., & Soffe, S. R. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1633-04.2004 · Cited by 117 · see citing works
GATA Proteins Identify a Novel Ventral Interneuron Subclass in the Developing Chick Spinal Cord
Karunaratne, A., Hargrave, M. R., Poh, A. M., & Yamada, T. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0754 · Cited by 107 · see citing works
Does the central pattern generation for locomotion in lamprey depend on glycine inhibition?
Grillner, S., & Wallén, P. (1980) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1980.tb06637.x · Cited by 104 · see citing works
Central Pattern Generators Deciphered by Molecular Genetics
Kiehn, O., & Kullander, K. (2004) · Neuron · doi:10.1016/s0896-6273(04)00042-x · Cited by 101 · see citing works
Self-citationActivity of commissural interneurons in spinal cord of Xenopus embryos
Soffe, S. R., Clarke, J., & Roberts, A. (1984) · Journal of Neurophysiology · doi:10.1152/jn.1984.51.6.1257 · Cited by 96 · see citing works
Localization of Spinal Neurons Activated During Locomotion Using thec-fosImmunohistochemical Method
Dai, X., Noga, B. R., Douglas, J. R., & Jordan, L. M. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00578.2004 · Cited by 95 · see citing works
Zhong, G., Sharma, K., & Harris‐Warrick, R. M. (2011) · Nature Communications · doi:10.1038/ncomms1276 · Cited by 95 · see citing works
Functional differentiation and organization of feline midlumbar commissural interneurones
Jankowska, E., Edgley, S. A., Krutki, P., & Hammar, I. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.083014 · Cited by 92 · see citing works
Avraham, O., Hadas, Y., Vald, L., Zisman, S., Schejter, A., Visel, A., & Klar, A. (2009) · Neural Development · doi:10.1186/1749-8104-4-21 · Cited by 88 · see citing works
Contralaterally projecting lamina VIII interneurones in middle lumbar segments in the cat
Jankowska, E., & Noga, B. R. (1990) · Brain Research · doi:10.1016/0006-8993(90)91618-q · Cited by 85 · see citing works
Bernhardt, N. R., Gezelius, H., Vallstedt, A., Memic, F., & Kullander, K. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5096-09.2009 · Cited by 84 · see citing works
Self-citationRetrograde Signaling onto Ret during Motor Nerve Terminal Maturation
Baudet, C., Pozas, E., Adameyko, I. I., Andersson, E., Ericson, J., & Ernfors, P. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4489-07.2008 · Cited by 71 · see citing works
Wenner, P., O'Donovan, M. J., & Matise, M. P. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.84.5.2651 · Cited by 70 · see citing works
Wallén‐Mackenzie, Å., Wootz, H., & Englund, H. (2010) · Upsala Journal of Medical Sciences · doi:10.3109/03009730903572073 · Cited by 59 · see citing works
Bernhardt, N. R., Memic, F., Gezelius, H., Thiebes, A. L., Vallstedt, A., & Kullander, K. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.03.017 · Cited by 53 · see citing works
Self-citationCoexpression of SCL and GATA3 in the V2 interneurons of the developing mouse spinal cord
Smith, E., Hargrave, M. R., Yamada, T., Begley, C. G., & Little, M. H. (2002) · Developmental Dynamics · doi:10.1002/dvdy.10093 · Cited by 52 · see citing works
Functional characterization of dI6 interneurons in the neonatal mouse spinal cord
Dyck, J. R. B., Lanuza, G. M., & Gosgnach, S. (2012) · Journal of Neurophysiology · doi:10.1152/jn.01132.2011 · Cited by 43 · see citing works
Dai, Y., Carlin, K. P., Li, Z., McMahon, D. G., Brownstone, R. M., & Jordan, L. M. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00265.2009 · Cited by 42 · see citing works
Genetics moving to neuronal networks
Kullander, K. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.03.001 · Cited by 36 · see citing works
Self-citationRole of glutamate in locomotor rhythm generating neuronal circuitry
Gezelius, H., Wallén‐Mackenzie, Å., Enjin, A., Lagerström, M. C., & Kullander, K. (2006) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2007.05.001 · Cited by 27 · see citing works
Self-citationNeurotransmitter systems of commissural interneurons in the lumbar spinal cord of neonatal rats
Wéber, I., Veress, G., Szűcs, P., Antal, M., & Birinyi, A. (2007) · Brain Research · doi:10.1016/j.brainres.2007.06.109 · Cited by 20 · see citing works
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A harmonized atlas of mouse spinal cord cell types and their spatial organization
Russ, D. E., Cross, R. B. P., Li, L., Koch, S. C., Matson, K. J. E., Yadav, A., Alkaslasi, M. R., Lee, D. I., Le Pichon, C. E., Menon, V., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25125-1 · Cited by 255 · see citing works
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Lu, D. C.-T., Niu, T., & Alaynick, W. A. (2015) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2015.00025 · Cited by 193 · see citing works
Rybak, I. A., Dougherty, K. J., & Shevtsova, N. A. (2015) · eNeuro · doi:10.1523/eneuro.0069-15.2015 · Cited by 173 · see citing works
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Zarkower, D. A., & Murphy, M. W. (2021) · Sexual Development · doi:10.1159/000518272 · Cited by 100 · see citing works
Lemieux, M., Josset, N., Roussel, M., Couraud, S., & Bretzner, F. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00042 · Cited by 79 · see citing works
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Ferrer, I. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.07.004 · Cited by 62 · see citing works
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Flynn, J. R., Conn, V. L., Boyle, K. A., Hughes, D. I., Watanabe, M., Velasquez, T., Goulding, M., Callister, R. J., & Graham, B. A. (2017) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2017.00005 · Cited by 57 · see citing works
Ziskind‐Conhaim, L., & Hochman, S. (2017) · Journal of Neurophysiology · doi:10.1152/jn.00322.2017 · Cited by 54 · see citing works
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Self-citationGorla, M., Santiago, C., Chaudhari, K., Layman, A. A. K., Oliver, P. M., & Bashaw, G. J. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.02.080 · Cited by 46 · see citing works
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The role of extracellular matrix in spinal cord development
Wiese, S., & Faissner, A. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.05.018 · Cited by 35 · see citing works
Laumonnerie, C., da Silva, R. V., Kania, A., & Wilson, S. I. (2014) · Development · doi:10.1242/dev.099606 · Cited by 35 · see citing works
Molecular mechanisms regulating axon responsiveness at the midline
Gorla, M., & Bashaw, G. J. (2020) · Developmental Biology · doi:10.1016/j.ydbio.2020.08.006 · Cited by 34 · see citing works
The mammalian spinal commissural system: properties and functions
Maxwell, D. J., & Soteropoulos, D. S. (2019) · Journal of Neurophysiology · doi:10.1152/jn.00347.2019 · Cited by 30 · see citing works
Rybak, I. A., Shevtsova, N. A., & Kiehn, O. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2013.261115 · Cited by 29 · see citing works
Dynamics and plasticity of spinal locomotor circuits
Manira, A. E. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.06.016 · Cited by 27 · see citing works
Hernández-Enríquez, B., Wu, Z., Martinez, E., Olsen, O., Kaprielian, Z., Maness, P. F., Yoshida, Y., Tessier‐Lavigne, M., & Tran, T. S. (2015) · Genes & Development · doi:10.1101/gad.268086.115 · Cited by 25 · see citing works
Neuronal Circuits That Control Rhythmic Pectoral Fin Movements in Zebrafish
Uemura, Y., Kato, K., Kawakami, K., Kimura, Y., Oda, Y., & Higashijima, S. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1484-20.2020 · Cited by 24 · see citing works
Heterogeneity in Oligodendroglia: Is it Relevant to Mouse Models and Human Disease?
Ornelas, I., McLane, L. E., Saliu, A., Evangelou, A., Khandker, L., & Wood, T. L. (2016) · Journal of Neuroscience Research · doi:10.1002/jnr.23900 · Cited by 21 · see citing works
Axonal Projection Patterns of the Dorsal Interneuron Populations in the Embryonic Hindbrain
Hirsch, D., Kohl, A., Wang, Y., & Sela‐Donenfeld, D. (2021) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2021.793161 · Cited by 15 · see citing works
Gorla, M., Chaudhari, K., Hale, M., Potter, C., & Bashaw, G. J. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.2491-21.2022 · Cited by 14 · see citing works
Motor hypertonia and lack of locomotor coordination in mutant mice lacking DSCAM
Lemieux, M., Laflamme, O. D., Thiry, L., Boulanger‐Piette, A., Frenette, J., & Bretzner, F. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00556.2015 · Cited by 14 · see citing works
Batista, C. M., Bianqui, L. L. T., Zanon, B. B., Ivo, M. M. A. A., de Oliveira, G. P., Maximino, J. R., & Chadi, G. (2014) · Neural Plasticity · doi:10.1155/2014/451639 · Cited by 12 · see citing works
González, A. B. I., Jakobsson, J. E. T., Vieillard, J., Lagerström, M. C., Kullander, K., & Boije, H. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.781197 · Cited by 11 · see citing works
Self-citationRodent Zic Genes in Neural Network Wiring
Herrera, E. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-981-10-7311-3_11 · Cited by 8 · see citing works
Unusual Quadrupedal Locomotion in Rat during Recovery from Lumbar Spinal Blockade of 5-HT7 Receptors
Sławińska, U., Majczyński, H., Kwaśniewska, A., Miazga, K., Cabaj, A. M., Bekisz, M., Jordan, L. M., & Zawadzka, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22116007 · Cited by 8 · see citing works
金山, 武., & Shirasaki, R. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24464 · Cited by 8 · see citing works
Yao, X., Zhang, K., Na, T., Wang, Y., Guo, Y., Xi, J., Li, X., Meng, S., & Xu, M. (2025) · Cell Death and Disease · doi:10.1038/s41419-025-07961-x · Cited by 6 · see citing works
Spinal dI4 Interneuron Differentiation From Human Pluripotent Stem Cells
Xu, J. L., Huang, L.-J., Fang, Z., Luo, H., Chen, Y.-Q., Li, Y., Gong, C.-Z., & Chen, H. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.845875 · Cited by 6 · see citing works
Molecular, genetic, cellular, and network functions in the spinal cord and brainstem
Stein, P. S. G. (2013) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12083 · Cited by 5 · see citing works
Locomotor Pattern Generation in the Rodent Spinal Cord
Harris‐Warrick, R. M. (2013) · Encyclopedia of Computational Neuroscience · doi:10.1007/978-1-4614-7320-6_48-1 · Cited by 5 · see citing works
NSAID-mediated cyclooxygenase inhibition disrupts ectodermal derivative formation in axolotl embryos
Marshall, E. J., Ramarapu, R., Leathers, T. A., Morrison‐Welch, N., Sandberg, K., Kawashima, M., & Rogers, C. D. (2025) · Differentiation · doi:10.1016/j.diff.2025.100856 · Cited by 4 · see citing works
Vertebrate spinal commissural neurons: a model system for studying axon guidance beyond the midline
Martinez, E. A., & Tran, T. S. (2015) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.173 · Cited by 3 · see citing works
Bernhardt, N. R., Memic, F., Velica, A., Tran, M. A., Vieillard, J., Sayyab, S., Chersa, T., Andersson, L., Whelan, P. J., Boije, H., et al. (2022) · eNeuro · doi:10.1523/eneuro.0518-21.2022 · Cited by 3 · see citing works
Self-citationFunctional Neuroanatomy of the Spinal Cord
Engelhardt, M., & Sobotzik, J.-M. (2017) · Springer eBooks · doi:10.1007/978-3-319-46293-6_2 · Cited by 3 · see citing works
Using mouse genetics to study the developing spinal locomotor circuit
Thiry, L., Roussel, M., Lemieux, M., & Bretzner, F. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-816477-8.00011-9 · Cited by 2 · see citing works
Development and Functional Anatomy of the Spine and Spinal Cord
Ko, H.-Y. (2019) · Springer eBooks · doi:10.1007/978-981-10-7033-4_2 · Cited by 2 · see citing works
Jagadeesan, S. K., Sandarage, R. V., & Tsai, E. C. (2026) · Frontiers in Neuroscience · doi:10.3389/fnins.2026.1745993 · Cited by 1 · see citing works
Development of the Human Spinal Cord
Ko, H.-Y. (2022) · Springer eBooks · doi:10.1007/978-981-19-0228-4_2 · Cited by 1 · see citing works
Auditory Sensing Systems: Overview
Denham, S. L. (2015) · Encyclopedia of Computational Neuroscience · doi:10.1007/978-1-4614-6675-8_764 · Cited by 1 · see citing works
Vertebrate Pattern Generation: Overview
Rybak, I. A. (2014) · Encyclopedia of Computational Neuroscience · doi:10.1007/978-1-4614-7320-6_758-1 · Cited by 1 · see citing works
Vertebrate Pattern Generation: Overview
Rybak, I. A., & Ausborn, J. (2022) · Encyclopedia of Computational Neuroscience · doi:10.1007/978-1-0716-1006-0_758 · Cited by 1 · see citing works
Factors influencing the spinal motoneurons in development
Wiese, S. (2015) · Neural Regeneration Research · doi:10.4103/1673-5374.169639
Connectivity of dI3 Interneurons In the Development of Mice Spinal Cord
Farah, C. (2017) · uO Research (University of Ottawa) · doi:10.20381/ruor-709
Characterization of WT1-expressing interneurons and investigation of their role in locomotion
Haque, F. (2019) · ERA: Education and Research Archive (University of Alberta) · doi:10.7939/r3-jt04-kz83
Bernhardt, N. R., Memic, F., Velica, A., Tran, M. A., Vieillard, J., Chersa, T., Andersson, L., Whelan, P. J., Boije, H., & Kullander, K. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.13.093799
Self-citationClinical and Functional Anatomy of the Spinal Cord
Ko, H.-Y., & Huh, S. (2021) · Springer eBooks · doi:10.1007/978-981-16-3679-0_1
Vertebrate Pattern Generation: Overview
Rybak, I. A., & Ausborn, J. (2019) · Encyclopedia of Computational Neuroscience · doi:10.1007/978-1-4614-7320-6_758-2
Locomotor Pattern Generation in the Rodent Spinal Cord
Harris‐Warrick, R. M. (2022) · Encyclopedia of Computational Neuroscience · doi:10.1007/978-1-0716-1006-0_48
Locomotor Pattern Generation in the Rodent Spinal Cord
Harris‐Warrick, R. M. (2015) · Encyclopedia of Computational Neuroscience · doi:10.1007/978-1-4614-6675-8_48
Vertebrate Pattern Generation: Overview
Rybak, I. A. (2015) · Encyclopedia of Computational Neuroscience · doi:10.1007/978-1-4614-6675-8_758
Chen, W.-J., Chen, D., Lin, S.-Y., Cai, G.-J., Li, W.-B., Deng, Z.-Y., Xie, Z.-H., Zhang, M., Han, C., & Li, Q. (2026) · Gene Reports · doi:10.1016/j.genrep.2026.102469
- Authors
- Vallstedt, A., & Kullander, K.
- Affiliations
- Uppsala University (SE)
- Corresponding author
- Kullander, Klas
- ORCID
- Kullander, Klas
- Venue
- Annals of the New York Academy of Sciences
- Publisher
- Wiley
- Published
- 2013-03
- Volume
- 1279
- Issue
- 1
- Pages
- 32-42
- ISSN
- 0077-8923 (ISSN-L)
- 1749-6632
- OpenAlex
- W1574524525
- Cited by
- 64
- References
- 76
- Citations by year
- 2026: 2 · 2025: 1 · 2022: 6 · 2021: 6 · 2020: 5 · 2019: 7 · 2018: 6 · 2017: 5 · 2016: 3 · 2015: 13 · 2014: 7 · 2013: 3
- FWCI
- 0.88
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Annals of the New York Academy of Sciences (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Royal Swedish Academy of Sciences
- Knut och Alice Wallenbergs Stiftelse
- Vetenskapsrådet
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- locomotor circuits, axon guidance, midline crossing, DMRT3, gait disturbance, neural circuit development
- MeSH terms
- Animals, Humans, Interneurons, Functional Laterality, Locomotion, Models, Biological, Motor Neurons, Nerve Net, Spinal Cord, Mice
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