Graded arrays of spinal and supraspinal V2a interneuron subtypes underlie forelimb and hindlimb motor control

Hayashi, Marito; Hinckley, Christopher A.; Driscoll, Shawn P.; Moore, Niall J.; Levine, Ariel J.; Hilde, Kathryn L.; Sharma, Kamal; Pfaff, Samuel L.

doi:10.1016/j.neuron.2018.01.023

Cited by 188Motor Control and AdaptationNeuroscience and Neuropharmacology ResearchNeurogenesis and neuroplasticity mechanisms

Graded arrays of spinal and supraspinal V2a interneuron subtypes underlie forelimb and hindlimb motor control

Open access

Hayashi, Marito, Hinckley, Christopher A., Driscoll, Shawn P., Moore, Niall J., Levine, Ariel J., Hilde, Kathryn L., Sharma, Kamal, Pfaff, Samuel L.·2018·Neuron

DOI 10.1016/j.neuron.2018.01.023PMC PMC8601153

Open this paper in CoChat — free account Open PDF

Abstract

The spinal cord contains neural networks that enable regionally distinct motor outputs along the body axis. Nevertheless, it remains unclear how segment-specific motor computations are processed because the cardinal interneuron classes that control motor neurons appear uniform at each level of the spinal cord. V2a interneurons are essential to both forelimb and hindlimb movements, and here we identify two major types that emerge during development: type I neurons marked by high Chx10 form recurrent networks with neighboring spinal neurons and type II neurons that downregulate Chx10 and project to supraspinal structures. Types I and II V2a interneurons are arrayed in counter-gradients, and this network activates different patterns of motor output at cervical and lumbar levels. Single-cell RNA sequencing (RNA-seq) revealed type I and II V2a neurons are each comprised of multiple subtypes. Our findings uncover a molecular and anatomical organization of V2a interneurons reminiscent of the orderly way motor neurons are divided into columns and pools.

Integrity signals

Registry

Crossref · 10.1016/j.neuron.2018.01.023

Cites

81 of 81 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

V2a interneurons consist of two major subgroups with different settling positions: a medial subgroup expressing Nfib and Neurod2, and a lateral subgroup expressing Shox2 and Zfhx3.
“V2a interneurons have recently been shown to consist of two major subgroups that have different settling positions: a medial subgroup that expresses Nfib and Neurod2, and a lateral subgroup that expresses Shox2 and Zfhx3 (Hayashi et al., 2018).”
From Single cell transcriptomics reveals spatial and temporal dynamics of gene expression in the developing mouse spinal cord (2019) · cites this paper as Hayashi et al., 2018
In the spinal cord, the birth date of spinal neurons has been shown to correlate with subtype identity and functional properties in several specific cases.
“In the spinal cord, the birth date of spinal neurons has been shown to correlate with subtype identity and functional properties in several specific cases (Hayashi et al., 2018; Hollyday and Hamburger, 1977; Sockanathan and Jessell, 1998; Stam et al., 2012; Tripodi et al., 2011).”
From Single cell transcriptomics reveals spatial and temporal dynamics of gene expression in the developing mouse spinal cord (2019) · cites this paper as Hayashi et al., 2018
Neuronal subtypes vary along the rostral caudal axis of the neural tube.
“In addition, neuronal subtypes vary along the rostral caudal axis of the neural tube (Hayashi et al., 2018; Philippidou and Dasen, 2013; Sweeney et al., 2018).”
From Single cell transcriptomics reveals spatial and temporal dynamics of gene expression in the developing mouse spinal cord (2019) · cites this paper as Hayashi et al., 2018
The prioritized neurons resembled developmentally defined V2a neurons located in the lumbar spinal cord.
“The prioritized neurons resembled developmentally defined V2a neurons located in the lumbar spinal cord35.”
From The neurons that restore walking after paralysis (2022) · cites this paper as [35]
These neurons originate from a subset of developmentally defined V2a neurons.
“These neurons originate from a subset of developmentally defined V2a neurons35,41–45, which describe a family of neuronal subpopulations distributed along the neuraxis35,41–45.”
From The neurons that restore walking after paralysis (2022) · cites this paper as [35]

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
Love, M. I., Huber, W., & Anders, S. (2014) · Genome Biology · doi:10.1186/s13059-014-0550-8 · Cited by 95,106 · see citing works
Fast and accurate short read alignment with Burrows-Wheeler transform
Li, H., & Durbin, R. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp324 · Cited by 58,607 · see citing works
<tt>edgeR</tt> : a Bioconductor package for differential expression analysis of digital gene expression data
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp616 · Cited by 41,364 · see citing works
voom: precision weights unlock linear model analysis tools for RNA-seq read counts
Law, C. W., Chen, Y., Shi, W., & Smyth, G. K. (2014) · Genome Biology · doi:10.1186/gb-2014-15-2-r29 · Cited by 6,155 · see citing works
ConsensusClusterPlus: a class discovery tool with confidence assessments and item tracking
Wilkerson, M. D., & Hayes, D. N. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq170 · Cited by 5,719 · see citing works
Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation
McCarthy, D. J., Chen, Y., & Smyth, G. K. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks042 · Cited by 5,195 · see citing works
On aims and methods of ethology
Tinbergen, N. (1963) · Zeitschrift für Tierpsychologie · doi:10.1111/j.1439-0310.1963.tb01161.x · Cited by 4,551 · see citing works
Neuronal specification in the spinal cord: inductive signals and transcriptional codes
Jessell, T. M. (2000) · Nature Reviews Genetics · doi:10.1038/35049541 · Cited by 2,089 · see citing works
SC3: consensus clustering of single-cell RNA-seq data
Kiselev, V. Y., Kirschner, K., Schaub, M. T., Andrews, T., Yiu, A., Chandra, T., Natarajan, K. N., Reik, W., Barahona, M., Green, A. R., et al. (2017) · Nature Methods · doi:10.1038/nmeth.4236 · Cited by 1,500 · see citing works
Pooling across cells to normalize single-cell RNA sequencing data with many zero counts
L. Lun, A. T., Bach, K., & Marioni, J. C. (2016) · Genome Biology · doi:10.1186/s13059-016-0947-7 · Cited by 1,108 · see citing works
Neurophysiology of locomotor automatism
Shik, M. L., & Orlovsky, G. N. (1976) · Physiological Reviews · doi:10.1152/physrev.1976.56.3.465 · Cited by 1,071 · see citing works
Pax6 Controls Progenitor Cell Identity and Neuronal Fate in Response to Graded Shh Signaling
Ericson, J., Rashbass, P., Schedl, A., Brenner‐Morton, S., Kawakami, A., van Heyningen, V., Jessell, T. M., & Briscoe, J. (1997) · Cell · doi:10.1016/s0092-8674(00)80323-2 · Cited by 1,044 · see citing works
Complex Movements Evoked by Microstimulation of Precentral Cortex
Graziano, M. S. A., Taylor, C. S. R., & Moore, T. (2002) · Neuron · doi:10.1016/s0896-6273(02)00698-0 · Cited by 921 · 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
Circuits controlling vertebrate locomotion: moving in a new direction
Goulding, M. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2608 · Cited by 777 · cited 7× · see citing works
“Numerous classes of spinal interneurons have been identified along the dorsoventral and mediolateral axes of the neural tube based on their combinatorial expression of transcription factors during development (Alaynick et al., 2011; Goulding, 2009; Jessell, 2000).”
Influential
Decoding the organization of spinal circuits that control locomotion
Kiehn, O. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.9 · Cited by 742 · see citing works
Computations Underlying the Execution of Movement: A Biological Perspective
Bizzi, E., Mussa-Ivaldi, F. A., & Giszter, S. F. (1991) · Science · doi:10.1126/science.1857964 · Cited by 681 · see citing works
The motor cell columns of the lumbo‐sacral spinal cord of the cat
Romanes, G. J. (1951) · The Journal of Comparative Neurology · doi:10.1002/cne.900940209 · Cited by 546 · see citing works
LIM homeodomain factors Lhx3 and Lhx4 assign subtype identities for motor neurons.
Sharma, K., Sheng, H. Z., Lettieri, K., Li, H., Karavanov, A., Potter, S., Westphal, H., & Pfaff, S. (1998) · Cell · doi:10.1016/s0092-8674(00)81704-3 · Cited by 461 · see citing works
Genetic Identification of Spinal Interneurons that Coordinate Left-Right Locomotor Activity Necessary for Walking Movements
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
A 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
Hox Genes: Choreographers in Neural Development, Architects of Circuit Organization
Philippidou, P., & Dasen, J. S. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.020 · Cited by 423 · see citing works
Cell-Type-Specific Control of Brainstem Locomotor Circuits by Basal Ganglia
Roseberry, T. K., Lee, A. M., Lalive, A. L., Wilbrecht, L., Bonci, A., & Kreitzer, A. C. (2016) · Cell · doi:10.1016/j.cell.2015.12.037 · Cited by 397 · see citing works
Measured motion: searching for simplicity in spinal locomotor networks
Grillner, S. E., & Jessell, T. M. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.10.011 · Cited by 380 · see citing works
LIM Factor Lhx3 Contributes to the Specification of Motor Neuron and Interneuron Identity through Cell-Type-Specific Protein-Protein Interactions
Thaler, J. P., Lee, S., Jurata, L. W., Gill, G. N., & Pfaff, S. L. (2002) · Cell · doi:10.1016/s0092-8674(02)00823-1 · Cited by 363 · see citing works
Genetic Ablation of V2a Ipsilateral Interneurons Disrupts Left-Right Locomotor Coordination in Mammalian Spinal Cord
Crone, 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
The locomotion of the low spinal cat. II. Interlimb coordination
Forssberg, H., Grillner, S. E., Halbertsma, J. M., & Rossignol, S. (1980) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1980.tb06534.x · Cited by 358 · see citing works
The distribution of motoneurones supplying chick hind limb muscles.
Landmesser, L. T. (1978) · The Journal of Physiology · doi:10.1113/jphysiol.1978.sp012545 · Cited by 356 · see citing works
Skilled reaching relies on a V2a propriospinal internal copy circuit
Azim, E., Jiang, J., Alstermark, B., & Jessell, T. M. (2014) · Nature · doi:10.1038/nature13021 · Cited by 355 · see citing works
Active suppression of interneuron programs within developing motor neurons revealed by analysis of homeodomain factor HB9
Thaler, J., Harrison, K., Sharma, K., Lettieri, K., Kehrl, J., & Pfaff, S. L. (1999) · Neuron · doi:10.1016/s0896-6273(01)80027-1 · Cited by 354 · see citing works
Dual-mode operation of neuronal networks involved in left–right alternation
Talpalar, A. E., Bouvier, J., Borgius, L., Fortin, G., Pierani, A., & Kiehn, O. (2013) · Nature · doi:10.1038/nature12286 · Cited by 345 · see citing works
Specification of Motor Neuron Identity by the MNR2 Homeodomain Protein
Tanabe, Y., William, C. M., & Jessell, T. M. (1998) · Cell · doi:10.1016/s0092-8674(00)81783-3 · Cited by 341 · 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
Functionally Related Motor Neuron Pool and Muscle Sensory Afferent Subtypes Defined by Coordinate ETS Gene Expression
Lin, J. H., Saito, T., Anderson, D. J., Lance-Jones, C. C., Jessell, T. M., & Arber, S. (1998) · Cell · doi:10.1016/s0092-8674(00)81770-5 · Cited by 334 · see citing works
Motor Circuits in Action: Specification, Connectivity, and Function
Arber, S. (2012) · Neuron · doi:10.1016/j.neuron.2012.05.011 · Cited by 303 · see citing works
<i>alx</i> , a Zebrafish Homolog of <i>Chx10</i> , Marks Ipsilateral Descending Excitatory Interneurons That Participate in the Regulation of Spinal Locomotor Circuits
Kimura, Y., Okamura, Y., & Higashijima, S.-I. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4993-05.2006 · Cited by 302 · see citing works
The Motor Pools of the Spinal Cord
Romanes, G. J. (1964) · Progress in brain research · doi:10.1016/s0079-6123(08)64045-5 · Cited by 281 · see citing works
Brainstem nucleus MdV mediates skilled forelimb motor tasks
Esposito, M. S., Capelli, P., & Arber, S. (2014) · Nature · doi:10.1038/nature13023 · Cited by 279 · 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
Spinal inhibitory interneuron diversity delineates variant motor microcircuits
Bikoff, J. B., Gabitto, M. I., Rivard, A. F., Drobac, E., Machado, T. A., Miri, A., Brenner-Morton, S., Famojure, E., Diaz, C., Alvarez, F. J., et al. (2016) · Cell · doi:10.1016/j.cell.2016.01.027 · Cited by 262 · see citing works
Descending command neurons in the brainstem that halt locomotion
Bouvier, J., Caggiano, V., Leiras, R., Caldeira, V., Bellardita, C., Balueva, K., Fuchs, A., & Kiehn, O. (2015) · Cell · doi:10.1016/j.cell.2015.10.074 · Cited by 259 · see citing works
Monosynaptic Rabies Virus Reveals Premotor Network Organization and Synaptic Specificity of Cholinergic Partition Cells
Stepien, A. E., Tripodi, M., & Arber, S. (2010) · Neuron · doi:10.1016/j.neuron.2010.10.019 · Cited by 246 · see citing works
Locomotor rhythm generation linked to the output of spinal Shox2 excitatory interneurons
Dougherty, K. J., Zagoraiou, L., Satoh, D., Rozani, I., Doobar, S., Arber, S., Jessell, T. M., & Kiehn, O. (2013) · Neuron · doi:10.1016/j.neuron.2013.08.015 · Cited by 229 · see citing works
Propriospinal Circuitry Underlying Interlimb Coordination in Mammalian Quadrupedal Locomotion
Juvin, L., Simmers, J., & Morin, D. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0696-05.2005 · Cited by 223 · see citing works
Identification of a cellular node for motor control pathways
Levine, A. J., Hinckley, C. A., Hilde, K. L., Driscoll, S. P., Poon, T., Montgomery, J. M., & Pfaff, S. L. (2014) · Nature Neuroscience · doi:10.1038/nn.3675 · Cited by 216 · 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
Optogenetic dissection reveals multiple rhythmogenic modules underlying locomotion
Hägglund, M., Dougherty, K. J., Borgius, L., Itohara, S., Iwasato, T., & Kiehn, O. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1304365110 · Cited by 183 · see citing works
Notch and MAML Signaling Drives Scl-Dependent Interneuron Diversity in the Spinal Cord
Peng, C., Yajima, H., Burns, C. E., Zon, L. I., Sisodia, S. S., Pfaff, S. L., & Sharma, K. (2007) · Neuron · doi:10.1016/j.neuron.2007.02.019 · Cited by 178 · see citing works
Phenotype of V2‐derived interneurons and their relationship to the axon guidance molecule EphA4 in the developing mouse spinal cord
Lundfald, L., Restrepo, C. E., Butt, S. J. B., Peng, C., Droho, S., Endo, T., Zeilhofer, H. U., Sharma, K., & Kiehn, O. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05906.x · Cited by 172 · see citing works
Electrophysiological Characterization of V2a Interneurons and Their Locomotor-Related Activity in the Neonatal Mouse Spinal Cord
Zhong, G., Droho, S., Crone, S. A., Dietz, S., Kwan, A. C., Webb, W. W., Sharma, K., & Harris-Warrick, R. M. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4849-09.2010 · Cited by 159 · see citing works
Spinal neurons reaching the lateral reticular nucleus as studied in the rat by retrograde transport of horseradish peroxidase
Menétrey, D., Roudier, F., & Besson, J. (1983) · The Journal of Comparative Neurology · doi:10.1002/cne.902200406 · Cited by 157 · see citing works
Locomotor-Like Rhythms in a Genetically Distinct Cluster of Interneurons in the Mammalian Spinal Cord
Hinckley, C. A., Hartley, R., Wu, L., Todd, A. J., & Ziskind‐Conhaim, L. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00647.2004 · Cited by 155 · see citing works
Distinct Cortical Circuit Mechanisms for Complex Forelimb Movement and Motor Map Topography
Harrison, T. C., Ayling, O. G. S., & Murphy, T. H. (2012) · Neuron · doi:10.1016/j.neuron.2012.02.028 · Cited by 154 · see citing works
Motor neurons control locomotor circuit function retrogradely via gap junctions
Song, J., Ampatzis, K., Björnfors, E. R., & Manira, A. E. (2016) · Nature · doi:10.1038/nature16497 · Cited by 146 · see citing works
Clarke's column neurons as the focus of a corticospinal corollary circuit
Hantman, A. W., & Jessell, T. M. (2010) · Nature Neuroscience · doi:10.1038/nn.2637 · Cited by 144 · see citing works
Firing and Cellular Properties of V2a Interneurons in the Rodent Spinal Cord
Dougherty, K. J., & Kiehn, O. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4821-09.2010 · Cited by 138 · see citing works
Heterogeneity of V2‐derived interneurons in the adult mouse spinal cord
Al‐Mosawie, A., Wilson, J. M. M., & Brownstone, R. M. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05907.x · Cited by 136 · see citing works
The C3–C4 propriospinal system in the cat and monkey: a spinal pre‐motoneuronal centre for voluntary motor control
Alstermark, B., Isa, T., Pettersson, L. ‐., & Sasaki, S. (2007) · Acta Physiologica · doi:10.1111/j.1748-1716.2006.01655.x · Cited by 135 · see citing works
Long-Distance Descending Spinal Neurons Ensure Quadrupedal Locomotor Stability
Ruder, L., Takeoka, A., & Arber, S. (2016) · Neuron · doi:10.1016/j.neuron.2016.10.032 · Cited by 128 · see citing works
Renshaw cell interneuron specialization is controlled by a temporally restricted transcription factor program
Stam, F. J., Hendricks, T. J., Zhang, J., Geiman, E. J., Francius, C., Labosky, P. A., Clotman, F., & Goulding, M. (2012) · Development · doi:10.1242/dev.071134 · Cited by 115 · cited 1× · see citing works
“Postmitotic spinal neurons are generated from progenitors over multiple days, and the timing of neurogenesis is often correlated with the appearance of different neuronal subtypes (Jessell, 2000; Stam et al., 2012; Tripodi et al., 2011).”
Motor-Circuit Communication Matrix from Spinal Cord to Brainstem Neurons Revealed by Developmental Origin
Pivetta, C., Esposito, M. S., Sigrist, M., & Arber, S. (2014) · Cell · doi:10.1016/j.cell.2013.12.014 · Cited by 106 · see citing works
Identification of multiple subsets of ventral interneurons and differential distribution along the rostrocaudal axis of the developing spinal cord
Francius, 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
Distribution of the mRNA encoding the four dopamine D1 receptor subtypes in the brain of the european eel (Anguilla anguilla): Comparative approach to the function of D1 receptors in vertebrates
Kapsimali, M., Vidal, B., González, A., Dufour, S., & Vernier, P. (2000) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(20000410)419:3 · Cited by 91 · see citing works
Trehalose-Enhanced Isolation of Neuronal Sub-Types from Adult Mouse Brain
Saxena, A., Wagatsuma, A., Noro, Y., Kuji, T., Asaka-Oba, A., Watahiki, A., Gurnot, C., Fagiolini, M., Hensch, T. K., & Carninci, P. (2012) · BioTechniques · doi:10.2144/0000113878 · Cited by 84 · see citing works
LMO4 Controls the Balance between Excitatory and Inhibitory Spinal V2 Interneurons
Joshi, K., Lee, S., Lee, J. W., Lee, S., & Lee, S. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.011 · Cited by 80 · see citing works
Characterization of Long Descending Premotor Propriospinal Neurons in the Spinal Cord
Ni, Y., Nawabi, H., Liu, X., Yang, L., Miyamichi, K., Tedeschi, A., Xu, B., Wall, N. R., Callaway, E. M., & He, Z. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1771-14.2014 · Cited by 75 · see citing works
Differences in the morphology of spinal V2a neurons reflect their recruitment order during swimming in larval zebrafish
Menelaou, E., VanDunk, C., & McLean, D. L. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23465 · Cited by 73 · see citing works
Motility in chick embryos with substitution of lumbosacral by brachial by lumbosacral spinal cord segments
Narayanan, C., & Hamburger, V. (1971) · Journal of Experimental Zoology · doi:10.1002/jez.1401780402 · Cited by 73 · 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
Distinct Limb and Trunk Premotor Circuits Establish Laterality in the Spinal Cord
Goetz, C., Pivetta, C., & Arber, S. (2014) · Neuron · doi:10.1016/j.neuron.2014.11.024 · Cited by 69 · see citing works
Irregular Breathing in Mice following Genetic Ablation of V2a Neurons
Crone, S. A., Viemari, J., Droho, S., Mrejeru, A., Ramirez, J., & Sharma, K. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0445-12.2012 · Cited by 66 · see citing works
Primacy of Flexor Locomotor Pattern Revealed by Ancestral Reversion of Motor Neuron Identity
Machado, T. A., Pnevmatikakis, E. A., Paninski, L., Jessell, T. M., & Miri, A. (2015) · Cell · doi:10.1016/j.cell.2015.06.036 · Cited by 63 · see citing works
Skill learning induced plasticity of motor cortical representations is time and age-dependent
Tennant, K. A., Adkins, D. L., Scalco, M. D., Donlan, N. A., Asay, A. L., Thomas, N. J., Kleim, J. A., & Jones, T. A. (2012) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2012.09.004 · Cited by 60 · see citing works
Spinal Locomotor Circuits Develop Using Hierarchical Rules Based on Motorneuron Position and Identity
Hinckley, C. A., Alaynick, W. A., Gallarda, B. W., Hayashi, M., Hilde, K. L., Driscoll, S. P., Dekker, J. D., Tucker, H. O., Sharpee, T. O., & Pfaff, S. L. (2015) · Neuron · doi:10.1016/j.neuron.2015.08.005 · Cited by 52 · see citing works
Chx10 Consolidates V2a Interneuron Identity through Two Distinct Gene Repression Modes
Clovis, Y. M., Seo, S. Y., Kwon, J.-S., Rhee, J. C., Yeo, S., Lee, J. W., Lee, S., & Lee, S. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.06.100 · Cited by 43 · see citing works
Satb2 Is Required for the Development of a Spinal Exteroceptive Microcircuit that Modulates Limb Position
Hilde, K. L., Levine, A. J., Hinckley, C. A., Hayashi, M., Montgomery, J. M., Gullo, M., Driscoll, S. P., Grosschedl, R., Kohwi, Y., Kohwi-Shigematsu, T., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.07.014 · Cited by 43 · see citing works
Self-citation
Columnar-Intrinsic Cues Shape Premotor Input Specificity in Locomotor Circuits
Bæk, M., Pivetta, C., Liu, J.-P., Arber, S., & Dasen, J. S. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.004 · Cited by 39 · see citing works
Cholinergic systems are essential for late-stage maturation and refinement of motor cortical circuits
Ramanathan, D., Conner, J. M., Anilkumar, A. A., & Tuszynski, M. H. (2014) · Journal of Neurophysiology · doi:10.1152/jn.00408.2014 · Cited by 22 · see citing works
Recombination of motor pattern generators
Grillner, S. (1991) · Current Biology · doi:10.1016/0960-9822(91)90066-6 · Cited by 20 · see citing works
Direct and indirect spino-cerebellar pathways: shared ideas but different functions in motor control
Jiang, J., Azim, E., Ekerot, C. ‐., & Alstermark, B. (2015) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2015.00075 · Cited by 17 · see citing works
Lack of topographical organisation of the corticospinal tract in the cervical spinal cord of the adult rat
Jeffery, N. D., & Fitzgerald, M. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01562-0 · Cited by 13 · see citing works

Flagged first, then by citations

Sorted by citations

Current principles of motor control, with special reference to vertebrate locomotion
Grillner, S., & El Manira, A. (2020) · Physiological Reviews · doi:10.1152/physrev.00015.2019 · Cited by 560 · see citing works
Massively Parallel Single Nucleus Transcriptional Profiling Defines Spinal Cord Neurons and Their Activity during Behavior
Sathyamurthy, A., Johnson, K. R., Matson, K. J. E., Dobrott, C. I., Li, L., Ryba, A. R., Bergman, T. B., Kelly, M. C., Kelley, M. W., & Levine, A. J. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.02.003 · Cited by 370 · see citing works
Single cell transcriptomics reveals spatial and temporal dynamics of gene expression in the developing mouse spinal cord
Delile, J., Rayon, T., Melchionda, M., Edwards, A., Briscoe, J., & Sagner, A. (2019) · Development · doi:10.1242/dev.173807 · Cited by 356 · see citing works
The neurons that restore walking after paralysis
Kathe, C., Skinnider, M. A., Hutson, T. H., Regazzi, N., Gautier, M., Demesmaeker, R., Komi, S., Ceto, S., James, N. D., Cho, N., et al. (2022) · Nature · doi:10.1038/s41586-022-05385-7 · Cited by 304 · see citing works
Transplanting neural progenitor cells to restore connectivity after spinal cord injury
Fischer, I., Dulin, J. N., & Lane, M. A. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-020-0314-2 · Cited by 297 · see citing works
Establishing neuronal diversity in the spinal cord: a time and a place
Sagner, A., & Briscoe, J. (2019) · Development · doi:10.1242/dev.182154 · Cited by 282 · see citing works
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
Self-citation
Progression in translational research on spinal cord injury based on microenvironment imbalance
Fan, B., Wei, Z., & Feng, S. (2022) · Bone Research · doi:10.1038/s41413-022-00199-9 · Cited by 248 · see citing works
Connecting circuits for supraspinal control of locomotion
Ferreira-Pinto, M. J., Ruder, L., Capelli, P., & Arber, S. (2018) · Neuron · doi:10.1016/j.neuron.2018.09.015 · Cited by 140 · see citing works
Recovery of walking after paralysis by regenerating characterized neurons to their natural target region
Squair, J. W., Milano, M., de Coucy, A., Gautier, M., Skinnider, M. A., James, N. D., Cho, N., Lasne, A., Kathe, C., Hutson, T. H., et al. (2023) · Science · doi:10.1126/science.adi6412 · Cited by 144 · see citing works
Roles of axon guidance molecules in neuronal wiring in the developing spinal cord
Chédotal, A. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0168-7 · Cited by 138 · see citing works
A 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
Conserved genetic signatures parcellate cardinal spinal neuron classes into local and projection subsets
Osseward, P. J., Amin, N. D., Moore, J. D., Temple, B. A., Barriga, B. K., Bachmann, L. C., Beltran, F., Gullo, M., Clark, R. C., Driscoll, S. P., et al. (2021) · Science · doi:10.1126/science.abe0690 · Cited by 115 · see citing works
Single-cell and spatial atlases of spinal cord injury in the Tabulae Paralytica
Skinnider, M. A., Gautier, M., Teo, A. Y. Y., Kathe, C., Hutson, T. H., Laskaratos, A., de Coucy, A., Regazzi, N., Aureli, V., James, N. D., et al. (2024) · Nature · doi:10.1038/s41586-024-07504-y · Cited by 131 · see citing works
The Neuroplastic and Therapeutic Potential of Spinal Interneurons in the Injured Spinal Cord
Zholudeva, L. V., Qiang, L., Marchenko, V., Dougherty, K. J., Sakiyama‐Elbert, S. E., & Lane, M. A. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.06.004 · Cited by 86 · see citing works
Cell 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
Multiple Rhythm-Generating Circuits Act in Tandem with Pacemaker Properties to Control the Start and Speed of Locomotion
Song, J., Pallucchi, I., Ausborn, J., Ampatzis, K., Bertuzzi, M., Fontanel, P., Picton, L. D., & El Manira, A. (2020) · Neuron · doi:10.1016/j.neuron.2019.12.030 · Cited by 84 · see citing works
Brainstem Circuits Controlling Action Diversification
Ruder, L., & Arber, S. (2019) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070918-050201 · Cited by 69 · see citing works
Sub-populations of Spinal V3 Interneurons Form Focal Modules of Layered Pre-motor Microcircuits
Chopek, J. W., Nascimento, F., Beato, M., Brownstone, R. M., & Zhang, Y. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.08.095 · Cited by 74 · see citing works
Hierarchical control of locomotion by distinct types of spinal V2a interneurons in zebrafish
Menelaou, E., & McLean, D. L. (2019) · Nature Communications · doi:10.1038/s41467-019-12240-3 · Cited by 73 · see citing works
Spinal Interneurons as Gatekeepers to Neuroplasticity after Injury or Disease
Zholudeva, L. V., Abraira, V. E., Satkunendrarajah, K., McDevitt, T. C., Goulding, M. D., Magnuson, D. S. K., & Lane, M. A. (2021) · The Journal of Neuroscience · doi:10.1523/jneurosci.1654-20.2020 · Cited by 74 · see citing works
Inhibition of HDAC increases BDNF expression and promotes neuronal rewiring and functional recovery after brain injury
Sada, N., Fujita, Y., Mizuta, N., Ueno, M., Furukawa, T., & Yamashita, T. (2020) · Cell Death and Disease · doi:10.1038/s41419-020-02897-w · Cited by 74 · see citing works
Descending motor circuitry required for NT-3 mediated locomotor recovery after spinal cord injury in mice
Han, Q., Ordaz, J. D., Liu, N., Richardson, Z., Wu, W., Xia, Y., Qu, W., Wang, Y., Dai, H., Zhang, Y. P., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-13854-3 · Cited by 73 · see citing works
The Functional Role of Spinal Interneurons Following Traumatic Spinal Cord Injury
Zavvarian, M.-M., Hong, J., & Fehlings, M. G. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00127 · Cited by 59 · see citing works
Molecular Logic of Spinocerebellar Tract Neuron Diversity and Connectivity
Baek, M., Menon, V., Jessell, T. M., Hantman, A. W., & Dasen, J. S. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.04.113 · Cited by 56 · see citing works
Motor primitives are determined in early development and are then robustly conserved into adulthood
Yang, Q., Logan, D., & Giszter, S. F. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1821455116 · Cited by 58 · see citing works
Spinal V2b neurons reveal a role for ipsilateral inhibition in speed control
Callahan, R. A., Roberts, R., Sengupta, M., Kimura, Y., Higashijima, S.-I., & Bagnall, M. W. (2019) · eLife · doi:10.7554/elife.47837 · Cited by 57 · see citing works
Spinal Interneurons: Diversity and Connectivity in Motor Control
Sengupta, M., & Bagnall, M. W. (2023) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-083122-025325 · Cited by 58 · see citing works
Direct 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
Optical neuromodulation at all scales: from nanomaterials to wireless optoelectronics and integrated systems
Karatum, O., Gwak, M.-J., Hyun, J., Önal, A., Koirala, G. R., Kim, T., & Nizamoğlu, S. (2023) · Chemical Society Reviews · doi:10.1039/d2cs01020h · Cited by 54 · see citing works
Spinal Shox2 interneuron interconnectivity related to function and development
Ha, N. T., & Dougherty, K. J. (2018) · eLife · doi:10.7554/elife.42519 · Cited by 53 · see citing works
Single-cell analysis of innate spinal cord regeneration identifies intersecting modes of neuronal repair
Saraswathy, V. M., Zhou, L., & Mokalled, M. H. (2024) · Nature Communications · doi:10.1038/s41467-024-50628-y · Cited by 49 · see citing works
The rhythm section: an update on spinal interneurons setting the beat for mammalian locomotion
Dougherty, K. J., & Ha, N. T. (2019) · Current Opinion in Physiology · doi:10.1016/j.cophys.2019.01.004 · Cited by 45 · see citing works
Role of Propriospinal Neurons in Control of Respiratory Muscles and Recovery of Breathing Following Injury
Jensen, V. N., Alilain, W. J., & Crone, S. A. (2020) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2019.00084 · Cited by 45 · see citing works
Cerebrospinal fluid-contacting neuron tracing reveals structural and functional connectivity for locomotion in the mouse spinal cord
Nakamura, Y., Kurabe, M., Matsumoto, M., Sato, T., Miyashita, S., Hoshina, K., Kamiya, Y., Tainaka, K., Matsuzawa, H., Ohno, N., et al. (2023) · eLife · doi:10.7554/elife.83108 · Cited by 47 · see citing works
Proprioception: Bottom-up directive for motor recovery after spinal cord injury
Takeoka, A. (2019) · Neuroscience Research · doi:10.1016/j.neures.2019.07.005 · Cited by 40 · see citing works
Pathologically mislocalised TDP-43 in upper motor neurons causes a die-forward spread of ALS-like pathogenic changes throughout the mouse corticomotor system
Reale, L. A., Dyer, M. S., Perry, S. E., Young, K. M., Dickson, T. C., Woodhouse, A., & Blizzard, C. A. (2023) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2023.102449 · Cited by 33 · see citing works
Differential Loss of Spinal Interneurons in a Mouse Model of ALS
Salamatina, A., Yang, J. H., Brenner‐Morton, S., Bikoff, J. B., Fang, L., Kintner, C. R., Jessell, T. M., & Sweeney, L. B. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.08.011 · Cited by 37 · see citing works
Integration 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
Molecular blueprints for spinal circuit modules controlling locomotor speed in zebrafish
Pallucchi, I., Bertuzzi, M., Madrid, D., Fontanel, P., Higashijima, S.-I., & El Manira, A. (2024) · Nature Neuroscience · doi:10.1038/s41593-023-01479-1 · Cited by 34 · see citing works
V2a Neurons Constrain Extradiaphragmatic Respiratory Muscle Activity at Rest
Jensen, V. N., Seedle, K., Turner, S. M., Lorenz, J. N., & Crone, S. A. (2019) · eNeuro · doi:10.1523/eneuro.0492-18.2019 · Cited by 35 · see citing works
Regionally Specific Human Pre-Oligodendrocyte Progenitor Cells Produce Both Oligodendrocytes and Neurons after Transplantation in a Chronically Injured Spinal Cord Rat Model after Glial Scar Ablation
Patil, N., Walsh, P., Carrabre, K., Holmberg, E. G., Lavoie, N., Dutton, J. R., & Parr, A. M. (2020) · Journal of Neurotrauma · doi:10.1089/neu.2020.7009 · 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
Current Concepts of Neural Stem/Progenitor Cell Therapy for Chronic Spinal Cord Injury
Suzuki, H., Imajo, Y., Funaba, M., Nishida, N., Sakamoto, T., & Sakai, T. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.794692 · Cited by 36 · see citing works
The Temporal Neurogenesis Patterning of Spinal p3–V3 Interneurons into Divergent Subpopulation Assemblies
Deska‐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
Onecut Factors and Pou2f2 Regulate the Distribution of V2 Interneurons in the Mouse Developing Spinal Cord
Harris, 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
A hidden threshold in motor neuron gene networks revealed by modulation of miR-218 dose
Amin, N. D., Senturk, G., Costaguta, G., Driscoll, S. P., O’Leary, B., Bonanomi, D., & Pfaff, S. L. (2021) · Neuron · doi:10.1016/j.neuron.2021.07.028 · Cited by 31 · see citing works
Neuroplasticity and regeneration after spinal cord injury
Punjani, N., Deska‐Gauthier, D., Hachem, L. D., Abramian, M., & Fehlings, M. G. (2023) · North American Spine Society Journal (NASSJ) · doi:10.1016/j.xnsj.2023.100235 · Cited by 30 · see citing works
Thoracic VGluT2+Spinal Interneurons Regulate Structural and Functional Plasticity of Sympathetic Networks after High-Level Spinal Cord Injury
Noble, B. T., Brennan, F. H., Wang, Y., Guan, Z., Mo, X., Schwab, J. M., & Popovich, P. G. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.2134-21.2022 · Cited by 30 · see citing works
Decoding cell type diversity within the spinal cord
Dobrott, C. I., Sathyamurthy, A., & Levine, A. J. (2019) · Current Opinion in Physiology · doi:10.1016/j.cophys.2018.11.006 · Cited by 26 · 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
Neural ensembles that encode nocifensive mechanical and heat pain in mouse spinal cord
Zhang, M., Kupari, J., Su, J., Magnusson, K. A., Hu, Y., Calvo-Enrique, L., Usoskin, D., Albisetti, G. W., Ceder, M. M., Henriksson, K., et al. (2025) · Nature Neuroscience · doi:10.1038/s41593-025-01921-6 · Cited by 26 · see citing works
Plasticity in Cervical Motor Circuits following Spinal Cord Injury and Rehabilitation
Walker, J., & Detloff, M. R. (2021) · Biology · doi:10.3390/biology10100976 · Cited by 26 · see citing works
Modular derivation of diverse, regionally discrete human posterior CNS neurons enables discovery of transcriptomic patterns
Iyer, N. R., Shin, J., Cuskey, S., Tian, Y., Nicol, N. R., Doersch, T. E., Seipel, F., McCalla, S. G., Roy, S., & Ashton, R. S. (2022) · Science Advances · doi:10.1126/sciadv.abn7430 · Cited by 28 · see citing works
Deep scRNA sequencing reveals a broadly applicable Regeneration Classifier and implicates antioxidant response in corticospinal axon regeneration
Kim, J. M., Saikia, J. M., Monte, K. M. A., Ha, E., Romaus‐Sanjurjo, D., Sanchez, J. J., Moore, A. X., Hernaiz-Llorens, M., Chavez‐Martinez, C. L., Agba, C. K., et al. (2023) · Neuron · doi:10.1016/j.neuron.2023.09.019 · Cited by 26 · see citing works
Topographical and cell type-specific connectivity of rostral and caudal forelimb corticospinal neuron populations
Carmona, L. M., Thomas, E. D., Smith, K. A., Tasic, B., Costa, R. M., & Nelson, A. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.113993 · Cited by 23 · see citing works
Large-Scale Analysis of the Diversity and Complexity of the Adult Spinal Cord Neurotransmitter Typology
Pedroni, A., & Ampatzis, K. (2019) · iScience · doi:10.1016/j.isci.2019.09.010 · Cited by 22 · see citing works
A micro-LED implant and technique for optogenetic stimulation of the rat spinal cord
Mondello, S. E., Pedigo, B. D., Sunshine, M. D., Fischedick, A. E., Horner, P. J., & Moritz, C. T. (2020) · Experimental Neurology · doi:10.1016/j.expneurol.2020.113480 · Cited by 21 · see citing works
A Hox Code Defines Spinocerebellar Neuron Subtype Regionalization
Coughlan, E., Garside, V. C., Wong, S. F. L., Liang, H., Kraus, D., Karmakar, K., Maheshwari, U., Rijli, F. M., Bourne, J. A., & McGlinn, E. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.10.048 · Cited by 21 · see citing works
Transformation of an early-established motor circuit during maturation in zebrafish
Pallucchi, I., Bertuzzi, M., Michel, J. J. C., Miller, A. C., & Manira, A. E. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110654 · Cited by 21 · see citing works
Single-cell RNA-sequencing of mammalian brain development: insights and future directions
Vinsland, E., & Linnarsson, S. (2022) · Development · doi:10.1242/dev.200180 · Cited by 20 · 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
Decoupling of timescales reveals sparse convergent CPG network in the adult spinal cord
Radosevic, M., Willumsen, A., Petersen, P. C., Lindén, H., Vestergaard, M., & Berg, R. W. (2019) · Nature Communications · doi:10.1038/s41467-019-10822-9 · Cited by 21 · see citing works
Intrinsic brainstem circuits comprised of Chx10-expressing neurons contribute to reticulospinal output in mice
Chopek, J. W., Zhang, Y., & Brownstone, R. M. (2021) · Journal of Neurophysiology · doi:10.1152/jn.00322.2021 · Cited by 17 · 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
De novo establishment of circuit modules restores locomotion after spinal cord injury in adult zebrafish
Huang, C., Wang, Z., Cheng, J., Zhu, Z., Guan, N. N., & Song, J. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111535 · Cited by 19 · see citing works
Spatial transcriptomics and single-nucleus RNA sequencing reveal a transcriptomic atlas of adult human spinal cord
Zhang, D., Chen, Y., Wei, Y., Chen, H., Wu, Y., Wu, L., Li, J., Ren, Q., Miao, C., Zhu, T., et al. (2024) · eLife · doi:10.7554/elife.92046.2 · Cited by 19 · see citing works
Pou2f2 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
V2a neurons restore diaphragm function in mice following spinal cord injury
Jensen, V. N., Huffman, E. E., Jalufka, F. L., Pritchard, A. L., Baumgartner, S., Walling, I. T., Gibbs, H. C., McCreedy, D. A., Alilain, W. J., & Crone, S. A. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2313594121 · Cited by 17 · see citing works
Temporal 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
The cis-regulatory logic integrating spatial and temporal patterning in the vertebrate neural tube
Zhang, I., Boezio, G. L. M., Cornwall-Scoones, J., Frith, T. J. R., Finnie, E., Luo, J., Jiang, M., Howell, M. T., Lovell-Badge, R. H., Sagner, A., et al. (2025) · Developmental Cell · doi:10.1016/j.devcel.2025.06.029 · Cited by 17 · see citing works
Derivation of Specific Neural Populations From Pluripotent Cells for Understanding and Treatment of Spinal Cord Injury
White, N., & Sakiyama‐Elbert, S. E. (2018) · Developmental Dynamics · doi:10.1002/dvdy.24680 · 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
Chx10+V2a interneurons in spinal motor regulation and spinal cord injury
Li, Z., Wang, Y., Li, W., Deng, L., Zhai, F., & Wang, X. (2022) · Neural Regeneration Research · doi:10.4103/1673-5374.355746 · Cited by 16 · see citing works
Developmental stage of transplanted neural progenitor cells influences anatomical and functional outcomes after spinal cord injury in mice
Aceves, M., Tucker, A., Chen, J., Vo, K., Moses, J., Kumar, P. A., Thomas, H., Miranda, D., Dampf, G., Dietz, V. A., et al. (2023) · Communications Biology · doi:10.1038/s42003-023-04893-0 · Cited by 13 · see citing works
Distinguishing subtypes of spinal locomotor neurons to inform circuit function and dysfunction
Dougherty, K. J. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102763 · Cited by 14 · see citing works
Spatial transcriptomics and single-nucleus RNA sequencing reveal a transcriptomic atlas of adult human spinal cord
Zhang, D., Chen, Y., Wei, Y., Chen, H., Wu, Y., Wu, L., Li, J., Ren, Q., Miao, C., Zhu, T., et al. (2023) · eLife · doi:10.7554/elife.92046 · Cited by 14 · see citing works
A brain-wide map of descending inputs onto spinal V1 interneurons
Chapman, P., Kulkarni, A. S., Trevisan, A. J., Han, K., Hinton, J. M., Deltuvaite, P., Fenno, L. E., Ramakrishnan, C., Patton, M. H., Schwarz, L. A., et al. (2024) · Neuron · doi:10.1016/j.neuron.2024.11.019 · Cited by 14 · see citing works
A Single Cell Atlas of Spared Tissue Below a Spinal Cord Injury Reveals Cellular Mechanisms of RepairPreprint
Matson, K. J. E., Russ, D. E., Kathe, C., Maric, D., Hua, I., Krynitsky, J., Pursley, R. H., Sathyamurthy, A., Squair, J. W., Courtine, G., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.04.28.441862 · Cited by 13 · see citing works
Transcriptome Profiling of miRNA-mRNA Interactions and Associated Mechanisms in Chemotherapy-Induced Neuropathic Pain
Yang, X.-H., Huang, X., Lu, W., Yan, F., Ye, Y., Wang, L., Tang, X., Zeng, W., Huang, J., & Xie, J. (2023) · Molecular Neurobiology · doi:10.1007/s12035-023-03398-5 · Cited by 12 · see citing works
Single-cell RNAseq analysis of spinal locomotor circuitry in larval zebrafish
Kelly, J. J., Wen, H., & Brehm, P. (2023) · eLife · doi:10.7554/elife.89338 · Cited by 12 · see citing works
Transcriptional control of motor pool formation and motor circuit connectivity by the LIM-HD protein Isl2
Lee, Y., Yeo, I. S., Kim, N., Lee, D.-K., Kim, K., Yoon, J.-Y., Yi, J., Hong, Y. B., Choi, B., Kosodo, Y., et al. (2023) · eLife · doi:10.7554/elife.84596 · Cited by 12 · see citing works
Stimulation of Single, Possible CHX10 Hindbrain Neurons Turns Swimming On and Off in Young Xenopus Tadpoles
Li, W., & Soffe, S. R. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00047 · Cited by 12 · see citing works
Establishing the Molecular and Functional Diversity of Spinal Motoneurons
Dasen, J. S. (2022) · Advances in neurobiology · doi:10.1007/978-3-031-07167-6_1 · Cited by 12 · see citing works
Cell Transplantation for Repair of the Spinal Cord and Prospects for Generating Region-Specific Exogenic Neuronal Cells
Roman, A., Huntemer-Silveira, A., Waldron, M. A., Khalid, Z., Blake, J., Parr, A. M., & Low, W. C. (2024) · Cell Transplantation · doi:10.1177/09636897241241998 · Cited by 11 · see citing works
Elevated phagocytic capacity directs innate spinal cord repair
Shaw, D. K., Saraswathy, V. M., McAdow, A. R., Zhou, L., Park, D., Mote, R. D., Saini, A., Douthitt, A. J., Stepankova, K., Unverzagt, B., et al. (2026) · Cell Reports · doi:10.1016/j.celrep.2026.117482 · 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
Single Cell Transcriptomic Analysis of Spinal Dmrt3 Neurons in Zebrafish and Mouse Identifies Distinct Subtypes and Reveal Novel Subpopulations Within the dI6 Domain
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
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
Nervous tract-bioinspired multi-nanoyarn model system regulating neural differentiation and its transcriptional architecture at single-cell resolution
Li, Z., Qi, Y., Li, Z., Chen, S., Geng, H., Han, J., Wang, J., Wang, Z., Sun, L., Huang, B., et al. (2023) · Biomaterials · doi:10.1016/j.biomaterials.2023.122146 · Cited by 11 · see citing works
Human spinal interneurons repair the injured spinal cord through synaptic integrationPreprint
Zholudeva, L. V., Fortino, T. A., Agrawal, A., Vila, O. F., Williams, M., McDevitt, T. C., Lane, M. A., & Srivastava, D. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.01.11.575264 · Cited by 11 · see citing works
Long-Term Cultures of Spinal Cord Interneurons
Vargová, I., Kriška, J., Kwok, J. C. F., Fawcett, J. W., & Jendelová, P. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.827628 · Cited by 10 · see citing works
Choosing the right cell for spinal cord repair
Zholudeva, L. V., & Lane, M. A. (2018) · Journal of Neuroscience Research · doi:10.1002/jnr.24351 · Cited by 10 · see citing works
Intersectional genetic tools to study skilled reaching in mice
Nicola, F., Hua, I., & Levine, A. J. (2021) · Experimental Neurology · doi:10.1016/j.expneurol.2021.113879 · Cited by 9 · see citing works
A fresh look at propriospinal interneurons plasticity and intraspinal circuits remodeling after spinal cord injury
Cheng, J., & Guan, N. N. (2023) · IBRO Neuroscience Reports · doi:10.1016/j.ibneur.2023.04.001 · Cited by 9 · see citing works
Origin and circuitry of spinal locomotor interneurons generating different speeds
Boije, H., & Kullander, K. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.04.024 · Cited by 9 · see citing works
Decoding Bilateral Hindlimb Kinematics From Cat Spinal Signals Using Three-Dimensional Convolutional Neural Network
Fathi, Y., & Erfanian, A. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.801818 · Cited by 9 · see citing works

Rostrocaudal Diversification of Spinal Neurons Confers Segment-Specific Spinal Network Architectures
Hayashi, M. (2016) · eScholarship (California Digital Library)
Hierarchical control of locomotion by distinct types of spinal V2a interneurons in zebrafish
Menelaou, E., & McLean, D. L. (2019) · Nature Communications · doi:10.1038/s41467-019-12240-3 · Cited by 73 · see citing works
V2a interneuron diversity tailors spinal circuit organization to control the vigor of locomotor movements
Song, J., Dahlberg, E., & El Manira, A. (2018) · Nature Communications · doi:10.1038/s41467-018-05827-9 · Cited by 64 · see citing works
Identification of multiple subsets of ventral interneurons and differential distribution along the rostrocaudal axis of the developing spinal cord
Francius, 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
Distinct Spinal V2a and V0d Microcircuits Distribute Locomotor Control in Larval ZebrafishPreprint
Menelaou, E., Kishore, S., & McLean, D. L. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/559799 · Cited by 2 · see citing works

Authors: Hayashi, M., Hinckley, C. A., Driscoll, S. P., Moore, N. J., Levine, A. J., Hilde, K. L., Sharma, K., & Pfaff, S. L.
Affiliations: Salk Institute for Biological Studies (US)
University of Illinois Chicago (US)
Corresponding author: Pfaff, Samuel L.
ORCID: Hayashi, Marito
Hinckley, Christopher A.
Driscoll, Shawn P.
Moore, Niall J.
Levine, Ariel J.
Hilde, Kathryn L.
Sharma, Kamal
Pfaff, Samuel L.
Venue: Neuron
Publisher: Elsevier BV
Published: 2018-02
Volume: 97
Issue: 4
Pages: 869-884.e5
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/j.neuron.2018.01.023
PMC: PMC8601153
OpenAlex: W2785626601
Cited by: 188
References: 81
Citations by year: 2026: 14 · 2025: 16 · 2024: 28 · 2023: 35 · 2022: 24 · 2021: 20 · 2020: 14 · 2019: 26 · 2018: 11
FWCI: 10.56
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 385 d)
Locations: Neuron (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: NIH-NCI CCSG (P30 014195)
NINDS R24 Core Grant
NEI
Chapman Foundation
Helmsley Charitable Trust
Japanese Ministry of Education, Culture, Sports, Science, and Technology Long-Term Student Support Program
Timken-Sturgis Foundation
NIH NINDS
George E. Hewitt Foundation for Medical Research
Christopher and Dana Reeve Foundation
NSF
Howard Hughes Medical Institute
Sol Goldman Charitable Trust
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords: V2a interneurons, spinal interneurons, Chx10, interneuron subtypes, interneuron development, motor pools, single-cell RNA sequencing
MeSH terms: Animals, Female, Forelimb, Hindlimb, Interneurons, Lumbosacral Region, Male, Mice, Inbred C57BL, Motor Neurons, Movement, Neural Pathways, Spinal Cord, Transcription Factors, Homeodomain Proteins, Cervical Cord

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

Graded arrays of spinal and supraspinal V2a interneuron subtypes underlie forelimb and hindlimb motor control

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks