Lbx1 specifies somatosensory association interneurons in the dorsal spinal cord
Open accessAbstract
Association and relay neurons that are generated in the dorsal spinal cord play essential roles in transducing somatosensory information. During development, these two major neuronal classes are delineated by the expression of the homeodomain transcription factor Lbx1. Lbx1 is expressed in and required for the correct specification of three early dorsal interneuron populations and late-born neurons that form the substantia gelatinosa. In mice lacking Lbx1, cells types that arise in the ventral alar plate acquire more dorsal identities. This results in the loss of dorsal horn association interneurons, excess production of commissural neurons, and disrupted sensory afferent innervation of the dorsal horn. Lbx1, therefore, plays a critical role in the development of sensory pathways in the spinal cord that relay pain and touch.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The increase in dI4 and dI5 neurons is explained by the expansion of the combined dp4/dp5 progenitor pool in the dorsal spinal cord at these stages and the extended phase of neurogenesis in the dorsal spinal cord that results in late born dI4 and dI5 neurons.
“This is explained by the expansion of the combined dp4/dp5 progenitor pool in the dorsal spinal cord at these stages and the extended phase of neurogenesis in the dorsal spinal cord that results in the formation of late born dI4 and dI5 neurons”
From Single cell transcriptomics reveals spatial and temporal dynamics of gene expression in the developing mouse spinal cord (2019) · cites this paper as Gross et al., 2002
The decrease in dorsal progenitors at e13.5 is in line with the higher rate of neurogenesis in the dorsal spinal cord at e13.5 and the consequent depletion of progenitors.
“This is in line with the higher rate of neurogenesis in the dorsal spinal cord at e13.5 and the consequent depletion of progenitors”
From Single cell transcriptomics reveals spatial and temporal dynamics of gene expression in the developing mouse spinal cord (2019) · cites this paper as Gross et al., 2002
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 [105]
Cites
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
The cytoarchitectonic organization of the spinal cord in the cat
Rexed, B. (1952) · The Journal of Comparative Neurology · doi:10.1002/cne.900960303 · Cited by 1,633 · see citing works
Sensory Mechanisms of the Spinal Cord
Willis, W. D., & Coggeshall, R. E. (1978) · Springer eBooks · doi:10.1007/978-1-4757-1688-7 · Cited by 1,456 · 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
Briscoe, J., Pierani, A., Jessell, T. M., & Ericson, J. (2000) · Cell · doi:10.1016/s0092-8674(00)80853-3 · Cited by 1,111 · see citing works
Sensory Mechanisms of the Spinal Cord
Willis, W. D., & Coggeshall, R. E. (1991) · Springer eBooks · doi:10.1007/978-1-4899-0597-0 · Cited by 934 · see citing works
Tackling Pain at the Source: New Ideas about Nociceptors
Snider, W. D., & McMahon, S. B. (1998) · Neuron · doi:10.1016/s0896-6273(00)81003-x · Cited by 853 · see citing works
Preserved Acute Pain and Reduced Neuropathic Pain in Mice Lacking PKCγ
Malmberg, A. B., Chen, C., Tonegawa, S., & Basbaum, A. I. (1997) · Science · doi:10.1126/science.278.5336.279 · Cited by 690 · see citing works
Liem, K. F., Tremml, G., & Jessell, T. M. (1997) · Cell · doi:10.1016/s0092-8674(01)80015-5 · Cited by 591 · see citing works
Organization in the Spinal Cord
Brown, A. G. (1981) · Springer eBooks · doi:10.1007/978-1-4471-1305-8 · Cited by 524 · see citing works
O’Gorman, S., Dagenais, N., Qian, M., & Marchuk, Y. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.26.14602 · Cited by 436 · see citing works
A sonic hedgehog-independent, retinoid-activated pathway of neurogenesis in the ventral spinal cord.
Pierani, A., Brenner-Morton, S., Chiang, C., & Jessell, T. (1999) · Cell · doi:10.1016/s0092-8674(00)80802-8 · Cited by 398 · 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
Self-citationMüller, 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
Neuronal and synaptic arrangement in the substantia gelatinosa rolandi
Szentágothai, J. (1964) · The Journal of Comparative Neurology · doi:10.1002/cne.901220207 · Cited by 359 · see citing works
Goulding, M., Lumsden, A., & Gruss, P. (1993) · Trends in Genetics · doi:10.1016/0168-9525(93)90082-s · Cited by 354 · see citing works
Self-citationLee, K. J., Mendelsohn, M. M., & Jessell, T. M. (1998) · Genes & Development · doi:10.1101/gad.12.21.3394 · Cited by 341 · see citing works
Goulding, M., Lumsden, A., & Gruß, P. (1993) · Development · doi:10.1242/dev.117.3.1001 · Cited by 335 · see citing works
Self-citationProprioceptor 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
Crossinhibitory Activities of Ngn1 and Math1 Allow Specification of Distinct Dorsal Interneurons
Gowan, K., Helms, A. W., Hunsaker, T., Collisson, T., Ebert, P. J., Odom, R., & Johnson, J. E. B. (2001) · Neuron · doi:10.1016/s0896-6273(01)00367-1 · Cited by 302 · see citing works
Dottori, M., Gross, M. K., Labosky, P. A., & Goulding, M. (2001) · Development · doi:10.1242/dev.128.21.4127 · Cited by 299 · 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
Lbx1 is required for muscle precursor migration along a lateral pathway into the limb
Gross, M. K., Moran-Rivard, L., Velasquez, T., Nakatsu, M. N., Jagla, K., & Goulding, M. (2000) · Development · doi:10.1242/dev.127.2.413 · Cited by 261 · see citing works
Self-citationEvx1 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
Self-citationKornhuber, H. H., & Albe-Fessard, D. (1975) · Medical Entomology and Zoology · Cited by 235 · 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
Self-citationWang, S. S., Tsai, R. Y. L., & Reed, R. R. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-11-04149.1997 · Cited by 210 · see citing works
Jagla, K., Dollé, P., Mattéi, M., et al. (1995) · Mechanisms of Development · doi:10.1016/0925-4773(95)00450-5 · Cited by 152 · see citing works
Rnx deficiency results in congenital central hypoventilation
Shirasawa, S., Arata, A., Onimaru, H., et al. (2000) · Nature Genetics · doi:10.1038/73516 · Cited by 150 · see citing works
Mansouri, A., & Gruss, P. (1998) · Mechanisms of Development · doi:10.1016/s0925-4773(98)00168-3 · Cited by 148 · see citing works
Antal, M., Polgár, E., Chalmers, J. P., Minson, J. B., Llewellyn‐Smith, I. J., Heizmann, C. W., & Somogyi, P. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903140111 · Cited by 143 · see citing works
Chen, Z., Rebelo, S., White, F. A., Malmberg, A. B., Baba, H., Lima, D., Woolf, C. J., Basbaum, A. I., & Anderson, D. J. (2001) · Neuron · doi:10.1016/s0896-6273(01)00341-5 · Cited by 133 · see citing works
Organization of the spinal cord
Eccles, J. C., & Schadé, J. P. (1964) · Cited by 131 · see citing works
Polgár, E., Shehab, S. A. S., Watt, C., & Todd, A. J. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-07-02637.1999 · Cited by 107 · see citing works
Early development of the circumferential axonal pathway in mouse and chick spinal cord
Holley, J. A. (1982) · The Journal of Comparative Neurology · doi:10.1002/cne.902050406 · Cited by 101 · see citing works
Saito, T., Greenwood, A. L., Sun, Q. L., et al. (1995) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.1995.1022 · Cited by 81 · see citing works
Pituello, F., Yamada, G., & Gruss, P. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.15.6952 · Cited by 63 · see citing works
Lbx1 marks a subset of interneurons in chick hindbrain and spinal cord
Schubert, F., Dietrich, S., Mootoosamy, R. C., Chapman, S. C., & Lumsden, A. (2001) · Mechanisms of Development · doi:10.1016/s0925-4773(00)00537-2 · Cited by 31 · see citing works
Li, Y., Li, H., Kaneko, T., et al. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01794-1 · Cited by 17 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
Self-citationIdentification of Spinal Circuits Transmitting and Gating Mechanical Pain
Duan, B., Cheng, L., Bourane, S., Britz, O., Padilla, C., Garcia-Campmany, L., Krashes, M., Knowlton, W., Velasquez, T., Ren, X., et al. (2014) · Cell · doi:10.1016/j.cell.2014.11.003 · Cited by 582 · see citing works
Self-citationCurrent 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
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
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
Stolt, C. C., Schlierf, A., Lommes, P., Hillgärtner, S., Werner, T., Kosian, T., Sock, E., Kessaris, N., Richardson, W. D., Lefebvre, V., et al. (2006) · Developmental Cell · doi:10.1016/j.devcel.2006.08.011 · Cited by 299 · see citing works
Zhang, J., Lanuza, G. M., Britz, O., Wang, Z., Siembab, V. C., Zhang, Y., Velasquez, T., Alvarez, F. J., Frank, E., & Goulding, M. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.013 · Cited by 233 · see citing works
Self-citationA 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
Ptf1a determines GABAergic over glutamatergic neuronal cell fate in the spinal cord dorsal horn
Glasgow, S. M., Henke, R. M., MacDonald, R. J., Wright, C. V. E., & Johnson, J. E. (2005) · Development · doi:10.1242/dev.02167 · Cited by 225 · see citing works
Identification of a Spinal Circuit for Light Touch and Fine Motor Control
Bourane, S., Grossmann, K. S., Britz, O., Dalet, A., Del Barrio, M. G., Stam, F. J., Garcia-Campmany, L., Koch, S., & Goulding, M. (2015) · Cell · doi:10.1016/j.cell.2015.01.011 · Cited by 215 · see citing works
Self-citationNormal and abnormal coding of somatosensory stimuli causing pain
Prescott, S. A., Ma, Q., & De Koninck, Y. (2014) · Nature Neuroscience · doi:10.1038/nn.3629 · Cited by 210 · see citing works
Making sense out of spinal cord somatosensory development
Lai, H. C., Seal, R. P., & Johnson, J. E. (2016) · Development · doi:10.1242/dev.139592 · Cited by 188 · see citing works
Ogura, T., Sakaguchi, H., Miyamoto, S., & Takahashi, J. (2018) · Development · doi:10.1242/dev.162214 · Cited by 183 · see citing works
The bHLH factor Olig3 coordinates the specification of dorsal neurons in the spinal cord
Müller, T., Anlag, K., Wildner, H., Britsch, S., Treier, M., & Birchmeier, C. (2005) · Genes & Development · doi:10.1101/gad.326105 · Cited by 150 · see citing works
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 · 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-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
The 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
Neuronal diversity in the somatosensory system: bridging the gap between cell type and function
Gatto, G., Smith, K. M., Ross, S. E., & Goulding, M. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2019.03.002 · Cited by 74 · see citing works
Self-citationDorsally derived spinal interneurons in locomotor circuits
Vallstedt, A., & Kullander, K. (2013) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2012.06801.x · Cited by 64 · see citing works
Recruitment of Spinoparabrachial Neurons by Dorsal Horn Calretinin Neurons
Petitjean, H., Bourojeni, F. B., Tsao, D., Davidova, A., Sotocinal, S. G., Mogil, J. S., Kania, A., & Sharif-Naeini, R. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.07.048 · Cited by 47 · see citing works
Spinal somatostatin-positive interneurons transmit chemical itch
Fatima, M., Ren, X., Pan, H., Slade, H. F. E., Asmar, A. J., Xiong, C. M., Shi, A., Xiong, A. E., Wang, L., & Duan, B. (2019) · Pain · doi:10.1097/j.pain.0000000000001499 · Cited by 41 · see citing works
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
Characterization of Foxp2-expressing cells in the developing spinal cord
Morikawa, Y., Hisaoka, T., & Senba, E. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.05.022 · Cited by 33 · see citing works
Spinal Inhibitory Ptf1a-Derived Neurons Prevent Self-Generated Itch
Escalante, A., & Klein, R. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108422 · Cited by 17 · see citing works
- Authors
- Gross, M. K., Dottori, M., & Goulding, M.
- Affiliations
- Salk Institute for Biological Studies (US)
- Corresponding author
- Goulding, Martyn
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2002-05
- Volume
- 34
- Issue
- 4
- Pages
- 535-549
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2082785396
- Cited by
- 396
- References
- 39
- Citations by year
- 2026: 9 · 2025: 8 · 2024: 10 · 2023: 21 · 2022: 14 · 2021: 13 · 2020: 15 · 2019: 18 · 2018: 19 · 2017: 15 · 2016: 18 · 2015: 16 · 2014: 17 · 2013: 24 · 2012: 22
- FWCI
- 4.95
- 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, 4095 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- 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 › Physiology › Pain Mechanisms and Treatments
- Keywords
- Lbx1, dorsal spinal cord, dorsal horn, substantia gelatinosa, homeodomain transcription factor, neuronal specification, commissural neurons, spinal cord development
- MeSH terms
- Afferent Pathways, Animals, Axons, Cell Differentiation, Cell Movement, Female, Interneurons, Male, Mice, Transgenic, Muscle Proteins, Mutation, Nerve Fibers, Nerve Fibers, Myelinated, Neural Pathways, Nociceptors, Substantia Gelatinosa, Transcription Factors, Apoptosis, Gene Expression Regulation, Developmental, Cell Lineage, Body Patterning, Posterior Horn Cells, Receptor, trkA, Mice
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