Neuronal diversity in the somatosensory system: bridging the gap between cell type and function
Open accessAbstract
A recent flurry of genetic studies in mice have provided key insights into how the somatosensory system is organized at a cellular level to encode itch, pain, temperature, and touch. These studies are largely predicated on the idea that functional cell types can be identified by their unique developmental provenance and gene expression profile. However, the extent to which gene expression profiles can be correlated with functional cell types and circuit organization remains an open question. In this review, we focus on recent progress in characterizing the sensory afferent and dorsal horn neuron cell types that process cutaneous somatosensory information and ongoing circuit studies that are beginning to bridge the divide between cell type and function.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Organoid neurons were reminiscent of NC-derived neurons found in cranial or dorsal root ganglia, with medium-large soma NEFH+PRPH+ neurons and smaller soma NEFH−PRPH+ neurons.
“The organoid neurons were reminiscent of NC-derived neurons found in cranial or dorsal root ganglia, with medium-large soma Neurofilament-Heavy Chain (NEFH)+ Peripherin (PRPH)+ neurons and smaller soma NEFH−PRPH+ neurons (Fig. 3o, Supplementary Video 7)23,31.”
From Hair-bearing human skin generated entirely from pluripotent stem cells (2020) · cites this paper as [31]
The “Sensory afferent heterogeneity” section describes neural-crest-derived trigeminal and dorsal root ganglion sensory neurons as having similar molecularly defined types. It mentions neurofilament as a historical sensory-afferent marker, but does not describe the claimed NEFH/PRPH combinations or their association with soma size. The organoid observations are the citing authors’ own results, not findings reported by this source. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe most salient neuronal morphology was consistent with NEFH+ pseudounipolar neurons, reminiscent of Aβ/δ-LTMRs or proprioceptors.
“The most salient neuronal morphology was consistent with NEFH+ pseudounipolar neurons, reminiscent of Aβ/δ-LTMRs or proprioceptors (Fig. 3m, n)31.”
From Hair-bearing human skin generated entirely from pluripotent stem cells (2020) · cites this paper as [31]
The “Sensory afferent heterogeneity” section (page unavailable) discusses neurofilament as a historical marker for skin afferents and identifies Aβ- and Aδ-LTMR populations. It does not describe NEFH+ pseudounipolar morphology or link that morphology to LTMRs or proprioceptors; the claim’s specific morphological identification is therefore unsupported by this copy. (LLM, conf=0.73)
Experimental — accuracy not yet measuredIn large ganglia (>10 neurons), a subset of Parvalbumin (PVALB)+ neuron somas was identified, indicative of proprioceptors.
“In large ganglia (>10 neurons), we identified a subset of Parvalbumin (PVALB)+ neuron somas, indicative of proprioceptors (Extended Data Fig. 7j)31.”
From Hair-bearing human skin generated entirely from pluripotent stem cells (2020) · cites this paper as [31]
The sensory-afferent heterogeneity section discusses ganglion sensory-neuron types, and the cellular-diversity section mentions proprioceptive transmission, but neither links PVALB-positive somas to proprioceptors. Searches for parvalbumin, PVALB and proprioceptors found no passage establishing that identification. The observation in large ganglia is the citing authors’ own result, not a finding attributed to this review. (LLM, conf=0.72)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Cellular and Molecular Mechanisms of Pain
Basbaum, A. I., Bautista, D. M., Scherrer, G., & Julius, D. (2009) · Cell · doi:10.1016/j.cell.2009.09.028 · Cited by 4,344 · see citing works
Molecular Architecture of the Mouse Nervous System
Zeisel, A., Hochgerner, H., Lönnerberg, P., Johnsson, A., Memic, F., van der Zwan, J., Häring, M., Braun, E., Borm, L. E., La Manno, G., et al. (2018) · Cell · doi:10.1016/j.cell.2018.06.021 · Cited by 2,995 · see citing works
Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing
Usoskin, D., Furlan, A., Islam, S., Abdo, H., Lönnerberg, P., Lou, D., Hjerling-Leffler, J., Haeggström, J., Kharchenko, O., Kharchenko, P. V., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.3881 · Cited by 2,136 · see citing works
Abraira, V. E., & Ginty, D. D. (2013) · Neuron · doi:10.1016/j.neuron.2013.07.051 · Cited by 1,648 · see citing works
Neuronal circuitry for pain processing in the dorsal horn
Todd, A. J. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2947 · Cited by 1,475 · see citing works
A gastrin-releasing peptide receptor mediates the itch sensation in the spinal cord
Sun, Y.-G., & Chen, Z. (2007) · Nature · doi:10.1038/nature06029 · Cited by 792 · see citing works
Identification 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-citationThe Cells and Circuitry for Itch Responses in Mice
Mishra, S. K., & Hoon, M. A. (2013) · Science · doi:10.1126/science.1233765 · Cited by 507 · see citing works
McGlone, F. P., & Reilly, D. M. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.08.004 · Cited by 470 · see citing works
Häring, M., Zeisel, A., Hochgerner, H., Rinwa, P., Jakobsson, J. E. T., Lönnerberg, P., La Manno, G., Sharma, N., Borgius, L., Kiehn, O., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0141-1 · Cited by 470 · see citing works
Li, C., Li, K., Wu, D., Chen, Y., Luo, H., Zhao, J., Wang, S.-S., Sun, M.-M., Lu, Y., Zhong, Y., et al. (2015) · Cell Research · doi:10.1038/cr.2015.149 · Cited by 452 · see citing works
Loss of Inhibitory Interneurons in the Dorsal Spinal Cord and Elevated Itch in Bhlhb5 Mutant Mice
Ross, S. E., Mardinly, A. R., McCord, A. E., Zurawski, J. D., Cohen, S., Jung, C. C., Hu, L. S., Mok, S. I., Shah, A., Savner, E. M., et al. (2010) · Neuron · doi:10.1016/j.neuron.2010.02.025 · Cited by 445 · see citing works
Self-citationThe Cellular and Synaptic Architecture of the Mechanosensory Dorsal Horn
Abraira, V. E., Kuehn, E. D., Chirila, A. M., Springel, M. W., Toliver, A. A., Zimmerman, A. L., Orefice, L. L., Boyle, K. A., Bai, L., Song, B. J., et al. (2017) · Cell · doi:10.1016/j.cell.2016.12.010 · Cited by 409 · 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
Self-citationPeripheral and Central Mechanisms of Itch
Dong, X., & Dong, X. (2018) · Neuron · doi:10.1016/j.neuron.2018.03.023 · Cited by 382 · see citing works
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
Dynorphin Acts as a Neuromodulator to Inhibit Itch in the Dorsal Horn of the Spinal Cord
Kardon, A. P., Polgár, E., Hachisuka, J., Snyder, L. M., Cameron, D., Savage, S., Cai, X., Karnup, S., Fan, C. R., Hemenway, G. M., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.046 · Cited by 369 · 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
Dorsal Horn Circuits for Persistent Mechanical Pain
Peirs, C., Williams, S.-P. G., Zhao, X., Walsh, C. E., Gedeon, J. Y., Cagle, N. E., Goldring, A. C., Hioki, H., Liu, Z., Marell, P. S., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.07.029 · Cited by 327 · see citing works
Dorsal Horn Parvalbumin Neurons Are Gate-Keepers of Touch-Evoked Pain after Nerve Injury
Petitjean, H., Pawlowski, S. A., Fraine, S. L., Sharif, B., Hamad, D., Fatima, T., Berg, J., Brown, C. M., Jan, L.-Y., Ribeiro-da-Silva, A., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.09.080 · Cited by 326 · see citing works
Gate control of mechanical itch by a subpopulation of spinal cord interneurons
Bourane, S., Duan, B., Koch, S. C., Dalet, A., Britz, O., Garcia-Campmany, L., Kim, E., Cheng, L., Ghosh, A., Ma, Q., et al. (2015) · Science · doi:10.1126/science.aac8653 · Cited by 296 · see citing works
Self-citationTouch and tactile neuropathic pain sensitivity are set by corticospinal projections
Liu, Y., Latremoliere, A., Li, X., Zhang, Z., Chen, M., Wang, X., Fang, C., Zhu, J., Alexandre, C., Gao, Z., et al. (2018) · Nature · doi:10.1038/s41586-018-0515-2 · Cited by 276 · see citing works
Circuit dissection of the role of somatostatin in itch and pain
Huang, J., Polgár, E., Solinski, H. J., Mishra, S. K., Tseng, P.-Y., Iwagaki, N., Boyle, K. A., Dickie, A. C., Kriegbaum, M. C., Wildner, H., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0119-z · Cited by 257 · see citing works
Single-cell RNAseq reveals seven classes of colonic sensory neuron
Hockley, J. R. F., Taylor, T. S., Callejo, G., Wilbrey, A. L., Gutteridge, A., Bach, K., Winchester, W. J., Bulmer, D. C., McMurray, G., & Smith, E. S. J. (2018) · Gut · doi:10.1136/gutjnl-2017-315631 · Cited by 251 · see citing works
Identification of spinal circuits involved in touch-evoked dynamic mechanical pain
Cheng, L., Duan, B., Huang, T., Zhang, Y., Chen, Y., Britz, O., Garcia-Campmany, L., Ren, X., Vong, L., Lowell, B. B., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4549 · Cited by 240 · see citing works
Self-citationPtf1a 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-citationAscl1 and Gsh1/2 control inhibitory and excitatory cell fate in spinal sensory interneurons
Mizuguchi, R., Kriks, S., Cordes, R., Gossler, A., Ma, Q., & Goulding, M. (2006) · Nature Neuroscience · doi:10.1038/nn1706 · Cited by 196 · see citing works
Self-citationMaking 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
Diversity amongst trigeminal neurons revealed by high throughput single cell sequencing
Nguyen, M. Q., Wu, Y., Bonilla, L. S., von Buchholtz, L. J., & Ryba, N. J. P. (2017) · PLoS ONE · doi:10.1371/journal.pone.0185543 · Cited by 168 · see citing works
The coding of cutaneous temperature in the spinal cord
Chen, R., Hoon, M. A., & Chen, X. (2016) · Nature Neuroscience · doi:10.1038/nn.4350 · Cited by 163 · see citing works
Leaky Gate Model: Intensity-Dependent Coding of Pain and Itch in the Spinal Cord
Sun, S., Xu, Q., Guo, C., Guan, Y., Liu, Q., & Dong, X. (2017) · Neuron · doi:10.1016/j.neuron.2017.01.012 · Cited by 154 · see citing works
Hughes, D. I., Sikander, S., Kinnon, C. M., Boyle, K. A., Watanabe, M., Callister, R. J., & Graham, B. A. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.235655 · Cited by 151 · see citing works
Wang, H., & Zylka, M. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3248-09.2009 · Cited by 145 · see citing works
Tonic inhibition of chronic pain by neuropeptide Y
Solway, B., Bose, S. C., Corder, G. F., Donahue, R. R., & Taylor, B. K. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1017719108 · Cited by 139 · see citing works
Bhlhb5 and Prdm8 form a repressor complex involved in neuronal circuit assembly
Ross, S. E., McCord, A. E., Jung, C., Atan, D., Mok, S. I., Hemberg, M., Kim, T.-K., Salogiannis, J., Hu, L., Cohen, S., et al. (2012) · Neuron · doi:10.1016/j.neuron.2011.09.035 · Cited by 137 · see citing works
Self-citationPeirs, C., Dallel, R., & Todd, A. J. (2020) · Journal of Neural Transmission · doi:10.1007/s00702-020-02159-1 · Cited by 131 · 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-citationHuang, M.-G., Huang, T., Xiang, Y., Xie, Z., Chen, Y., Yan, R., Xu, J., & Cheng, L.-P. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.06.031 · Cited by 99 · see citing works
Stereotyped transcriptomic transformation of somatosensory neurons in response to injury
Nguyen, M. Q., Pichon, C. E. L., & Ryba, N. J. P. (2019) · eLife · doi:10.7554/elife.49679 · Cited by 99 · see citing works
Neuropeptide Y and its Involvement in Chronic Pain
Diaz‐delCastillo, M., Woldbye, D. P. D., & Heegaard, A. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.08.050 · Cited by 94 · see citing works
Boyle, K. A., Gutierrez-Mecinas, M., Polgár, E., Mooney, N., O'Connor, E., Furuta, T., Watanabe, M., & Todd, A. J. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.08.044 · Cited by 92 · see citing works
Bröhl, D., Strehle, M., Wende, H., Hori, K., Bormuth, I., Nave, K., Müller, T. H., & Birchmeier, C. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.08.002 · Cited by 90 · see citing works
Smith, K. M., Boyle, K. A., Madden, J. F., Dickinson, S. A., Jobling, P., Callister, R. J., Hughes, D. I., & Graham, B. A. (2015) · The Journal of Physiology · doi:10.1113/jp270855 · Cited by 88 · see citing works
Self-citationGutierrez-Mecinas, M., Furuta, T., Watanabe, M., & Todd, A. J. (2016) · Molecular Pain · doi:10.1177/1744806916629065 · Cited by 81 · see citing works
In Vivo Interrogation of Spinal Mechanosensory Circuits
Christensen, A. J., Iyer, S. M., François, A., Vyas, S., Ramakrishnan, C., Vesuna, S., Deisseroth, K., Scherrer, G., & Delp, S. L. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.10.010 · Cited by 75 · see citing works
Dickie, A. C., Bell, A. M., Iwagaki, N., Polgár, E., Gutièrrez‐Mecinas, M., Kelly, R., Lyon, H., Turnbull, K., West, S. J., Etlin, A., et al. (2018) · Pain · doi:10.1097/j.pain.0000000000001406 · Cited by 72 · see citing works
Barrio, M. G. D., Bourane, S., Grossmann, K. S., Schüle, R., Britsch, S., O’Leary, D. D. M., & Goulding, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077928 · Cited by 65 · see citing works
Self-citationOntogeny of Excitatory Spinal Neurons Processing Distinct Somatic Sensory Modalities
Xu, Y., Lopes, C., Wende, H., Guo, Z., Cheng, L., Birchmeier, C., & Ma, Q. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.5512-12.2013 · Cited by 63 · see citing works
Transcriptional Profiling of Somatostatin Interneurons in the Spinal Dorsal Horn
Chamessian, A. G., Young, M. N., Qadri, Y. J., Berta, T., Ji, R., & de Ven, T. V. (2018) · Scientific Reports · doi:10.1038/s41598-018-25110-7 · Cited by 54 · see citing works
Wildner, H., Gupta, R. D. D., Bröhl, D., Heppenstall, P., Zeilhofer, H., & Birchmeier, C. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0491-13.2013 · Cited by 48 · see citing works
Iwagaki, N., Ganley, R. P., Dickie, A. C., Polgár, E., Hughes, D. I., del Río, P., Revina, Y., Watanabe, M., Todd, A. J., & Riddell, J. S. (2015) · Pain · doi:10.1097/j.pain.0000000000000407 · Cited by 44 · see citing works
Hu, J., Huang, T., Li, T., Guo, Z., & Cheng, L.-P. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.6239-11.2012 · Cited by 41 · see citing works
Szabo, N. E., da Silva, R. V., Sotocinal, S. G., Zeilhofer, H. U., Mogil, J. S., & Kania, A. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4690-14.2015 · Cited by 39 · see citing works
Gong, N., Hagopian, G. G., Holmes, T. C., Luo, Z. D., & Xu, X. (2019) · eNeuro · doi:10.1523/eneuro.0272-19.2019 · Cited by 16 · see citing works
Insight into B5-I spinal interneurons and their role in the inhibition of itch and pain
Chiang, M. C., Hachisuka, J., Todd, A. J., & Ross, S. E. (2015) · Pain · doi:10.1097/j.pain.0000000000000474 · Cited by 16 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Transcriptional Reprogramming of Distinct Peripheral Sensory Neuron Subtypes after Axonal Injury
Renthal, W. R., Tochitsky, I., Yang, L., Cheng, Y., Li, E., Kawaguchi, R., Geschwind, D. H., & Woolf, C. J. (2020) · Neuron · doi:10.1016/j.neuron.2020.07.026 · Cited by 544 · see citing works
Hair-bearing human skin generated entirely from pluripotent stem cells
Lee, J., Rabbani, C. C., Gao, H., Steinhart, M. R., Woodruff, B. M., Pflum, Z. E., Kim, A., Heller, S., Liu, Y., Shipchandler, T. Z., et al. (2020) · Nature · doi:10.1038/s41586-020-2352-3 · Cited by 487 · 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
Single-nucleus transcriptomic analysis of human dorsal root ganglion neurons
Nguyen, M. Q., von Buchholtz, L. J., Reker, A. N., Ryba, N. J. P., & Davidson, S. (2021) · eLife · doi:10.7554/elife.71752 · Cited by 231 · see citing works
Mechanical Allodynia Circuitry in the Dorsal Horn Is Defined by the Nature of the Injury
Peirs, C., Williams, S.-P. G., Zhao, X., Arokiaraj, C. M., Ferreira, D. W., Noh, M.-C., Smith, K. M., Halder, P., Corrigan, K. A., Gedeon, J. Y., et al. (2021) · Neuron · doi:10.1016/j.neuron.2020.10.027 · Cited by 190 · see citing works
Self-citationCutaneous innervation in impaired diabetic wound healing
Nowak, N. C., Menichella, D. M., Miller, R., & Paller, A. S. (2021) · Translational research · doi:10.1016/j.trsl.2021.05.003 · Cited by 144 · see citing works
Peirs, C., Dallel, R., & Todd, A. J. (2020) · Journal of Neural Transmission · doi:10.1007/s00702-020-02159-1 · Cited by 131 · see citing works
Oncostatin M can sensitize sensory neurons in inflammatory pruritus
Tseng, P., & Hoon, M. A. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.abe3037 · Cited by 111 · see citing works
A spinoparabrachial circuit defined by Tacr1 expression drives pain
Barik, A., Sathyamurthy, A., Thompson, J., Seltzer, M., Levine, A., & Chesler, A. (2021) · eLife · doi:10.7554/elife.61135 · Cited by 93 · see citing works
A Functional Topographic Map for Spinal Sensorimotor Reflexes
Gatto, G., Bourane, S., Ren, X., Di Costanzo, S., Fenton, P. K., Halder, P., Seal, R. P., & Goulding, M. D. (2021) · Neuron · doi:10.1016/j.neuron.2020.10.003 · Cited by 92 · see citing works
Self-citationStereotyped transcriptomic transformation of somatosensory neurons in response to injury
Nguyen, M. Q., Pichon, C. E. L., & Ryba, N. J. P. (2019) · eLife · doi:10.7554/elife.49679 · Cited by 99 · see citing works
Decoding Cellular Mechanisms for Mechanosensory Discrimination
von Buchholtz, L. J., Ghitani, N., Lam, R. M., Licholai, J. A., Chesler, A. T., & Ryba, N. J. P. (2020) · Neuron · doi:10.1016/j.neuron.2020.10.028 · Cited by 89 · see citing works
Control of Mammalian Locomotion by Somatosensory Feedback
Frigon, A., Akay, T., & Prilutsky, B. I. (2021) · Comprehensive physiology · doi:10.1002/cphy.c210020 · Cited by 91 · see citing works
Building inner ears: recent advances and future challenges for in vitro organoid systems
van der Valk, W. H., Steinhart, M. R., Zhang, J., & Koehler, K. R. (2020) · Cell Death and Differentiation · doi:10.1038/s41418-020-00678-8 · Cited by 72 · see citing works
Zhang, C., Hu, M., Wang, X., Cui, X., Liu, J., Huang, Q., Cao, X., Zhou, F., Qian, J. X., He, S.-Q., et al. (2022) · eLife · doi:10.7554/elife.76063 · Cited by 64 · see citing works
Presynaptic Inhibition of Pain and Touch in the Spinal Cord: From Receptors to Circuits
Comitato, A., & Bardoni, R. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22010414 · Cited by 57 · see citing works
Spinal Inhibitory Interneurons: Gatekeepers of Sensorimotor Pathways
Stachowski, N. J., & Dougherty, K. J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22052667 · Cited by 51 · see citing works
Mrgprd Cre lineage neurons mediate optogenetic allodynia through an emergent polysynaptic circuit
Warwick, C. A., Cassidy, C., Hachisuka, J., Wright, M. C., Baumbauer, K. M., Adelman, P. C., Lee, K. H., Smith, K. M., Sheahan, T. D., Ross, S. E., et al. (2021) · Pain · doi:10.1097/j.pain.0000000000002227 · Cited by 45 · see citing works
Self-citationInteractions between skin-resident dendritic and Langerhans cells and pain-sensing neurons
Wilcox, N. C., Taheri, G., Halievski, K., Talbot, S., Silva, J. R., & Ghasemlou, N. (2024) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2024.03.006 · Cited by 44 · see citing works
Akay, T., & Murray, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22031467 · Cited by 47 · see citing works
von Buchholtz, L. J., Lam, R. M., Emrick, J. J., Chesler, A. T., & Ryba, N. J. P. (2020) · Pain · doi:10.1097/j.pain.0000000000001911 · Cited by 43 · see citing works
Degenerate neuronal and circuit mechanisms important for generating rhythmic motor patterns
Calabrese, R. L., & Marder, E. E. (2024) · Physiological Reviews · doi:10.1152/physrev.00003.2024 · Cited by 36 · 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
New light on cortical neuropeptides and synaptic network plasticity
Smith, S. J., Hawrylycz, M., Rossier, J., & Sümbül, U. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.04.002 · Cited by 26 · see citing works
Gupta, R. R. D., Scheurer, L., Pelczar, P., Wildner, H., & Zeilhofer, H. U. (2021) · Scientific Reports · doi:10.1038/s41598-021-84667-y · Cited by 27 · see citing works
Single-cell transcriptomic profiling of dorsal root ganglion: an overview
Xie, K., Xu, C., Zhu, T., & Zhang, D. (2023) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2023.1162049 · 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
Computational Modeling of Spinal Locomotor Circuitry in the Age of Molecular Genetics
Ausborn, J., Shevtsova, N. A., & Danner, S. M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22136835 · Cited by 24 · see citing works
Sensory Feedback Control of Locomotor Pattern Generation in Cats and Mice
Akay, T. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.05.008 · Cited by 22 · see citing works
Tools for Efficient Analysis of Neurons in a 3d Reference Atlas of Whole Mouse Spinal Cord
Fiederling, F., Hammond, L. A., Ng, D., Mason, C. A., & Dodd, J. (2021) · Cell Reports Methods · doi:10.1016/j.crmeth.2021.100074 · Cited by 22 · see citing works
Wu, Y. C., Temple, B. A., Sevilla, N., Zhang, J., Zhu, H., Zolotavin, P., Jin, Y., Duarte, D., Sanders, E., Azim, E., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114199 · Cited by 20 · see citing works
Chemogenetics: drug-controlled gene therapies for neural circuit disorders
Sternson, S. M., & Bleakman, D. (2020) · Cell and Gene Therapy Insights · doi:10.18609/cgti.2020.112 · Cited by 20 · see citing works
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
Ma, H., Gao, T., Jakobsson, J. E. T., Weman, H. M., Xu, B., Larhammar, D., & Lagerström, M. C. (2019) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.119.262584 · Cited by 18 · see citing works
Schorscher-Petcu, A., Takács, F., & Browne, L. E. (2021) · eLife · doi:10.7554/elife.62026 · Cited by 17 · see citing works
Control of Mammalian Locomotion by Somatosensory Feedback
Frigon, A., Akay, T., & Prilutsky, B. I. (2021) · Comprehensive physiology · doi:10.1002/j.2040-4603.2022.tb00203.x · Cited by 17 · see citing works
Gong, N., Hagopian, G. G., Holmes, T. C., Luo, Z. D., & Xu, X. (2019) · eNeuro · doi:10.1523/eneuro.0272-19.2019 · Cited by 16 · see citing works
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
Chang, S.-H., Su, Y., Chang, M., & Chen, J. (2021) · eLife · doi:10.7554/elife.63768 · Cited by 15 · see citing works
A neural progenitor mitotic wave is required for asynchronous axon outgrowth and morphology
Lacoste, J., Soula, H. A., Burg, A., Audibert, A., Darnat, P., Gho, M., & Louvet‐Vallée, S. (2022) · eLife · doi:10.7554/elife.75746 · Cited by 14 · see citing works
Role of DSCAM in the Development of Neural Control of Movement and Locomotion
Lemieux, M., Thiry, L., Laflamme, O. D., & Bretzner, F. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22168511 · Cited by 13 · see citing works
Sinha, G. P., Prasoon, P., Smith, B. N., & Taylor, B. K. (2021) · The Journal of Physiology · doi:10.1113/jp281033 · Cited by 10 · see citing works
Kosugi, A., Kudo, M., Inoue, K., Takada, M., & Seki, K. (2025) · iScience · doi:10.1016/j.isci.2025.112178 · Cited by 7 · see citing works
Garcia-Ramirez, D. L., Singh, S., McGrath, J. R., Ha, N. T., & Dougherty, K. J. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.957084 · Cited by 8 · see citing works
Rancic, V., Haque, F., Ballanyi, K., & Gosgnach, S. (2019) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2019.05.010 · Cited by 4 · see citing works
Sensational developments in somatosensory development?
Kania, A. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.12.011 · Cited by 5 · see citing works
Beyond lidocaine: selective voltage-gated sodium channel blockade for vaginal pain
Holland, R. A., & Ross, S. E. (2020) · Pain · doi:10.1097/j.pain.0000000000002037 · Cited by 5 · see citing works
Self-citationMartynyuk, T., Ricard, J., Bracchi-Ricard, V. C., Price, S., McGrath, J. R., Dougherty, K. J., Tom, V. J., & Bethea, J. R. (2024) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.10.021 · Cited by 4 · see citing works
Sensory Symphonies: How Excitatory Spinal Cord Modules Orchestrate Behavior
Gradwell, M. A., & Abraira, V. E. (2021) · Neuron · doi:10.1016/j.neuron.2020.12.012 · Cited by 4 · see citing works
Kókai, É., Luz, L. L., Fernandes, E. C., Safronov, B. V., Poisbeau, P., & Szűcs, P. (2022) · The Journal of Comparative Neurology · doi:10.1002/cne.25413 · Cited by 3 · see citing works
Innovations in spinal cord cell type heterogeneity across vertebrate evolutionPreprint
Ignatyev, Y., Papadopoulos, S., Soretić, M., Yeung, J., Lin, T., Tanaka, E. M., Peshkin, L., Levine, A. J., Gabitto, M. I., & Sweeney, L. B. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.10.09.680955 · Cited by 3 · see citing works
Jancsó, G., Dux, M., & Sántha, P. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms262110350 · Cited by 2 · see citing works
Zhang, D., Chen, Y., Wei, Y., Chen, H., Wu, Y., Wu, L., Li, J., Ren, Q., Miao, C., Zhu, T., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.09.26.559582 · Cited by 2 · see citing works
Identification of VGLUT3-expressing LTMRs-recruited spinal circuits for itch inhibition
Su, X., Wang, L., Liu, X., & Zhang, Y. (2025) · Molecular Brain · doi:10.1186/s13041-025-01245-3 · Cited by 1 · see citing works
Production of AAVs and Injection into the Spinal Cord
Wildner, H., Paterna, J., & Haenraets, K. (2022) · Neuromethods · doi:10.1007/978-1-0716-2039-7_19 · Cited by 1 · see citing works
Using Viral Vectors to Visualize Pain-Related Neural Circuits in Mice
Chen, B., Takatoh, J., & Wang, F. (2022) · Neuromethods · doi:10.1007/978-1-0716-2039-7_12 · Cited by 1 · see citing works
Channelrhodopsin-2 Assisted Circuit Mapping in the Spinal Cord Dorsal Horn
Smith, K. M., & Graham, B. A. (2022) · Neuromethods · doi:10.1007/978-1-0716-2039-7_18 · Cited by 1 · see citing works
Self-citationWarwick, C. A., Cassidy, C., Hachisuka, J., Wright, M. C., Baumbauer, K. M., Adelman, P. C., Lee, K. H., Smith, K. M., Ross, S. E., & Koerber, H. R. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.09.17.296384 · Cited by 1 · see citing works
Self-citationZhang, 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.92046.1 · Cited by 1 · see citing works
Neuron Type-Specific Translatomes in Spinal Cords of Naïve and Neuropathic MicePreprint
Gupta, R. R. D., Scheurer, L., Pelczar, P., Ralvenius, W. T., Wildner, H., & Zeilhofer, H. U. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.03.19.996645
Bradke, F., & Lin, T.-C. (2020) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.736725514.793570163
Cellular and molecular aspects of locomotion in insects
Gruhn, M., Cristina, G. D., Gorostiza, E. A., & Büschges, A. (2025) · Elsevier eBooks · doi:10.1016/b978-0-323-95424-2.00019-4
Development of the spinocerebellar system within the precerebellar network
Lai, H. C. (2026) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2026.01.013
Pyridin-2(1H)one derivatives - a new class of therapeutics for trigeminal pain
Murail, P. (2024) · theses.fr (ABES) · doi:10.70675/ad8d129azce02z4a4dz9aa8zea61b5651e61
Delta-opioïd receptor : a potential new target for migraine and headache therapies
Dussol, M. (2023) · theses.fr (ABES) · doi:10.70675/b5bbe422z1fabz4af3z9105z1a22963c1217
Blue plaque review series: Thomas Graham Brown: Before his time
Calabrese, R. L., & Marder, E. E. (2026) · Experimental Physiology · doi:10.1113/ep093413
Боміхов, О. В., Yarynka, V. V., Petriv, T. I., Melikov, Z. K., Voitenko, N. V., Medvediev, V. V., & Belan, P. V. (2026) · Ukrainian Neurosurgical Journal · doi:10.25305/unj.354660
McGrath, J. R., & Dougherty, K. J. (2026) · Frontiers in Neural Circuits · doi:10.3389/fncir.2026.1854977
Xiang, W., Khajeh, R., Delgado, K., Liu, J., Holtrup, A. A., Zhang, Q., Cameron, S., Nguyen, T., Bae, J. A., Halageri, A., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.09.27.754843
- Authors
- Gatto, G., Smith, K. M., Ross, S. E., & Goulding, M.
- Affiliations
- Salk Institute for Biological Studies (US)
- University of Pittsburgh (US)
- Corresponding author
- Ross, Sarah Elizabeth
- Goulding, Martyn
- Venue
- Current Opinion in Neurobiology
- Publisher
- Elsevier BV
- Published
- 2019-06
- Volume
- 56
- Pages
- 167-174
- ISSN
- 0959-4388 (ISSN-L)
- PMC
- PMC6583900
- OpenAlex
- W2935076193
- Cited by
- 74
- References
- 56
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 6 · 2023: 8 · 2022: 7 · 2021: 22 · 2020: 16 · 2019: 5
- FWCI
- 2.16
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Current Opinion in Neurobiology (acceptedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- N.I.H. (NS080586, NS086372, AR063772, NS 096705)
- EMBO (ALTF 13-2015)
- Salk Women in Science
- DSF Charitable Foundation
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
- Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
- Life Sciences › Neuroscience › Cognitive Neuroscience › Tactile and Sensory Interactions
- Keywords
- somatosensory system, dorsal horn neurons, neuronal cell types, pruritus, pain, thermosensation, touch, skin sensation, gene expression profiles, mouse genetics
- MeSH terms
- Animals, Neurons, Pain, Pruritus, Touch
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
