Subpopulations of gabaergic neurons in laminae i–iii of rat spinal dorsal horn defined by coexistence with classical transmitters, peptides, nitric oxide synthase or parvalbumin
Abstract
GABAergic neurons in laminae I-III of the spinal dorsal horn may contain one or more of the following compounds: glycine, acetylcholine, neuropeptide Y, enkephalin, nitric oxide synthase or parvalbumin. Although the pattern of co-localization of some of these compounds is understood, it is not known which types of GABAergic neurons contain parvalbumin, or whether nitric oxide synthase coexists with peptides, acetylcholine or parvalbumin in any of these neurons, and in this study we have used immunocytochemistry and enzyme histochemistry to resolve these issues. Parvalbumin-immunoreactivity was restricted to those GABA-immunoreactive neurons that also showed glycine-immunoreactivity and was not co-localized with neuropeptide Y-immunoreactivity or NADPH diaphorase activity. By combining NADPH diaphorase histochemistry with immunocytochemistry with an antiserum to nitric oxide synthase, we were able to show that NADPH diaphorase activity was a reliable marker for nitric oxide synthase in the spinal cord. Neurons that possess GABA- but not glycine-immunoreactivity may contain neuropeptide Y, enkephalin, acetylcholine or NADPH diaphorase, and all of the cholinergic neurons appear to contain NADPH diaphorase. By combining immunofluorescent detection of neuropeptide Y or enkephalin with NADPH diaphorase histochemistry, we showed that peptide-immunoreactivity did not coexist with NADPH diaphorase. This suggests that neither of these peptides coexists with nitric oxide synthase or wit…
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The Chat dorsal inhibitory cluster Inhib-14 was a deep dorsal (lamina 4), inhibitory and cholinergic population that also expressed Nos1.
“The Chat dorsal inhibitor cluster Inhib-14 was a deep dorsal (lamina 4), inhibitory and cholinergic population and also expressed Nos180–82.”
From A harmonized atlas of mouse spinal cord cell types and their spatial organization (2021) · cites this paper as [80]
Cites
Neuronal NADPH diaphorase is a nitric oxide synthase.
Hope, B. T., Michael, G. J., Knigge, K. M., & Vincent, S. R. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.7.2811 · Cited by 1,908 · see citing works
Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues.
Dawson, T. M., Bredt, D. S., Fotuhi, M., Hwang, P. M., & Snyder, S. H. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.17.7797 · Cited by 1,843 · 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
Bredt, D. S., Glatt, C. E., Hwang, P. M., Fotuhi, M., Dawson, T. M., & Snyder, S. H. (1991) · Neuron · doi:10.1016/0896-6273(91)90374-9 · Cited by 1,359 · see citing works
Calcium-binding proteins in the nervous system
Baimbridge, K. G., Celio, M. R., & ROGERS, J. H. (1992) · Trends in Neurosciences · doi:10.1016/0166-2236(92)90081-i · Cited by 1,336 · see citing works
GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus
Freund, T. F., & Antal, M. (1988) · Nature · doi:10.1038/336170a0 · Cited by 1,283 · see citing works
Nitric oxide (NO) and nociceptive processing in the spinal cord
Meller, S. T., & Gebhart, G. F. (1993) · Pain · doi:10.1016/0304-3959(93)90124-8 · Cited by 952 · see citing works
Houser, C. R., Crawford, G. D., Barber, R. P., Salvaterra, P. M., & Vaughn, J. E. (1983) · Brain Research · doi:10.1016/0006-8993(83)91312-4 · Cited by 748 · see citing works
The nitric oxide and cGMP signal transduction system: regulation and mechanism of action
Schmidt, H. H. H. W., Lohmann, S. M., & Walter, U. (1993) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/0167-4889(93)90006-b · Cited by 742 · see citing works
Self-citationParvalbumin in Most γ-Aminobutyric Acid-Containing Neurons of the Rat Cerebral Cortex
Celio, M. R. (1986) · Science · doi:10.1126/science.3945815 · Cited by 740 · see citing works
Schmidt, H. H. H. W., Gagné, G. D., Nakane, M., Pollock, J. S., MILLER, M. F., & Murad, F. (1992) · Journal of Histochemistry & Cytochemistry · doi:10.1177/40.10.1382087 · Cited by 610 · see citing works
Self-citationHendry, S. H. C., Jones, E. G., Emson, P. C., Lawson, D. E. M., Heizmann, C. W., & Streit, P. (1989) · Experimental Brain Research · doi:10.1007/bf00247904 · Cited by 512 · see citing works
Self-citationTodd, A. J., & Sullivan, A. C. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902960312 · Cited by 501 · see citing works
Self-citationIntracellular calcium-binding proteins: more sites than insights
Heizmann, C. W., & Hunzlker, W. (1991) · Trends in Biochemical Sciences · doi:10.1016/0968-0004(91)90041-s · Cited by 454 · see citing works
Self-citationBarber, R. P., Phelps, P. E., Houser, C. R., Crawford, G. D., Salvaterra, P. M., & Vaughn, J. E. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902290305 · Cited by 453 · see citing works
Kosaka, T., Tauchi, M., & Dahl, J. L. (1988) · Experimental Brain Research · doi:10.1007/bf00247609 · Cited by 417 · see citing works
Changes in Ca2+-binding proteins in human neurodegenerative disorders
Heizmann, C. W., & Braun, K. A. (1992) · Trends in Neurosciences · doi:10.1016/0166-2236(92)90067-i · Cited by 409 · see citing works
Self-citationSerotonergic control of the hippocampus via local inhibitory interneurons.
Freund, T. F., Gulyás, A. I., Acsády, L., Görcs, T. J., & Tóth, K. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.21.8501 · Cited by 360 · see citing works
Antisera to gamma-aminobutyric acid. I. Production and characterization using a new model system.
Hodgson, A. J., Penke, B., Erdei, A., Chubb, I. W., & Somogyi, P. (1985) · Journal of Histochemistry & Cytochemistry · doi:10.1177/33.3.3973378 · Cited by 344 · see citing works
Todd, A. J., & SPIKE, R. C. (1993) · Progress in Neurobiology · doi:10.1016/0301-0082(93)90045-t · Cited by 330 · see citing works
Self-citationNADPH diaphorase in the spinal cord of rats
Valtschanoff, J. G., Weinberg, R. J., & Rustioni, A. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903210204 · Cited by 321 · see citing works
Glycine immunoreactivity localized in the cochlear nucleus and superior olivary complex
Wenthold, R. J., Huie, D., Altschuler, R. A., & Reeks, K. A. (1987) · Neuroscience · doi:10.1016/0306-4522(87)92968-x · Cited by 309 · see citing works
Mizukawa, K., Vincent, S. R., McGeer, P. L., & McGeer, E. G. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902790210 · Cited by 293 · see citing works
Somogyi, P., Hodgson, A. J., Chubb, I. W., Penke, B., & Erdei, A. (1985) · Journal of Histochemistry & Cytochemistry · doi:10.1177/33.3.2579123 · Cited by 290 · see citing works
GABA-immunoreactive neurons in the dorsal horn of the rat spinal cord
Todd, A. J., & McKenzie, J. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90442-9 · Cited by 279 · see citing works
Self-citationNitric oxide synthase immunoreactivity in the rat, mouse, cat and squirrel monkey spinal cord
Dun, N. J., Dun, S. L., Wu, S., Förstermann, U., Schmidt, H. H. H. W., & Tseng, L. F. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90579-5 · Cited by 276 · see citing works
Self-citationThomas, E., & Pearse, A. G. E. (1964) · Acta Neuropathologica · doi:10.1007/bf00684399 · Cited by 227 · see citing works
Blottner, D., & Baumgarten, H. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903160105 · Cited by 222 · see citing works
Anderson, C. R. (1992) · Neuroscience Letters · doi:10.1016/0304-3940(92)90571-n · Cited by 205 · see citing works
Nitric oxide synthase immunoreactivity in rat spinal cord
Dun, N. J., Dun, S. L., Förstermann, U., & Tseng, L. F. (1992) · Neuroscience Letters · doi:10.1016/0304-3940(92)90599-3 · Cited by 190 · see citing works
Coexistence of NADPH diaphorase with GABA, glycine, and acetylcholine in rat spinal cord
SPIKE, R. C., Todd, A. J., & Johnston, H. M. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903350303 · Cited by 169 · see citing works
Self-citationAntal, M., Freund, T. F., & Polgár, E. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902950310 · Cited by 156 · see citing works
Kosaka, T., & Heizmann, C. W. (1989) · Brain Research · doi:10.1016/0006-8993(89)90048-6 · Cited by 153 · see citing works
Self-citationTopography of choline acetyltransferase Immunoreactive Neurons and fibers in the rat spinal cord
Borges, L. F., & Iversen, S. D. (1986) · Brain Research · doi:10.1016/0006-8993(86)91407-1 · Cited by 145 · see citing works
Nitric oxide synthase and GABA colocalize in lamina II of rat spinal cord
Valtschanoff, J. G., Weinberg, R. J., Rustioni, A., & Schmidt, H. H. H. W. (1992) · Neuroscience Letters · doi:10.1016/0304-3940(92)90791-5 · Cited by 145 · see citing works
Self-citationAntal, 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
Self-citationKägi, U., Berchtold, M. W., & Heizmann, C. W. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)48238-5 · Cited by 141 · see citing works
Self-citationRibeiro‐da‐Silva, A., & Cuello, A. C. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902950303 · Cited by 134 · see citing works
Rowan, S., Todd, A. J., & SPIKE, R. C. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90218-5 · Cited by 112 · see citing works
Self-citationLauterborn, J. C., Isackson, P. J., Montalvo, R., & Gall, C. M. (1993) · Molecular Brain Research · doi:10.1016/0169-328x(93)90073-x · Cited by 101 · see citing works
Lee, J., Price, R. H., Williams, F. G., Mayer, B., & Beitz, A. J. (1993) · Brain Research · doi:10.1016/0006-8993(93)91474-7 · Cited by 94 · see citing works
Characterization and immunocytochemical application of monoclonal antibodies against enkephalins.
Cuello, A. C., Milstein, C., Couture, R., Wright, B., Priestley, J. V., & Jarvis, J. (1984) · Journal of Histochemistry & Cytochemistry · doi:10.1177/32.9.6086744 · Cited by 94 · see citing works
Immunocytochemical study of somatostatin, neurotensin, GABA, and glycine in rat spinal dorsal horn
Proudlock, F. A., SPIKE, R. C., & Todd, A. J. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903270210 · Cited by 92 · see citing works
Self-citationTodd, A. J., SPIKE, R. C., Russell, G., & Johnston, H. M. (1992) · Brain Research · doi:10.1016/0006-8993(92)90888-g · Cited by 90 · see citing works
Self-citationCarr, P. A., Yamamoto, T., Karmy, G., Baimbridge, K. G., & Nagy, J. I. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90216-9 · Cited by 83 · see citing works
Todd, A. J. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90093-4 · Cited by 79 · see citing works
Self-citationFöhr, U. G., Weber, B. R., Müntener, M., Staudenmann, W., Hughes, G. J., Frutiger, S., Banville, D., Schäfer, B. W., & Heizmann, C. W. (1993) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1993.tb18084.x · Cited by 78 · see citing works
Self-citationYoshida, S., Senba, E., Kubota, Y., Hagihira, S., Yoshiya, I., Emson, P. C., & Tohyama, M. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90113-i · Cited by 64 · see citing works
Todd, A., Spike, R., Price, R. F., & Neilson, M. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-02-00774.1994 · Cited by 64 · see citing works
Self-citationYamamoto, T., Carr, P. A., Baimbridge, K. G., & Nagy, J. I. (1989) · Brain Research Bulletin · doi:10.1016/0361-9230(89)90195-0 · Cited by 63 · see citing works
Light and electron microscope study of GABA‐immunoreactive neurones in Lamina III of rat spinal cord
Powell, J. J., & Todd, A. J. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903150202 · Cited by 55 · see citing works
Self-citationTodd, A. J., Russell, G., & SPIKE, R. C. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90176-3 · Cited by 48 · see citing works
Self-citationCa2+-binding site of carp parvalbumin recognized by monoclonal antibody
Tinner, R., Oertle, M., Heizmann, C. W., & Bosshard, H. R. (1990) · Cell Calcium · doi:10.1016/0143-4160(90)90045-v · Cited by 36 · see citing works
Self-citationCoexistence of parvalbumin and glycine in the rat brainstem
Aoki, E., Semba, R., Seto‐Ohshima, A., Heizmann, C. W., & Kashiwamata, S. (1990) · Brain Research · doi:10.1016/0006-8993(90)91329-f · Cited by 30 · see citing works
Self-citationDoyle, C. A., & Maxwell, D. J. (1993) · Brain Research · doi:10.1016/0006-8993(93)91315-j · Cited by 23 · see citing works
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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
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
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
Foster, E., Wildner, H., Tudeau, L., Haueter, S., Ralvenius, W. T., Jegen, M., Johannssen, H. C., Hösli, L., Haenraets, K., Ghanem, A., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.02.028 · Cited by 350 · 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
Yasaka, T., Tiong, S. Y. X., Hughes, D. I., Riddell, J. S., & Todd, A. J. (2010) · Pain · doi:10.1016/j.pain.2010.08.008 · Cited by 315 · 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
Increased Abundance of Opioid Receptor Heteromers After Chronic Morphine Administration
Gupta, A., Mulder, J., Gomes, I., Rozenfeld, R., Bushlin, I., Ong, E. W., Lim, M. P., Maillet, É. L., Junek, M., Cahill, C. M., et al. (2010) · Science Signaling · doi:10.1126/scisignal.2000807 · Cited by 226 · see citing works
Identifying functional populations among the interneurons in laminae I-III of the spinal dorsal horn
Todd, A. J. (2017) · Molecular Pain · doi:10.1177/1744806917693003 · Cited by 204 · see citing works
Self-citationPrescott, S. A., & Koninck, Y. D. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2001.013437 · Cited by 204 · see citing works
The types of neuron which contain protein kinase C gamma in rat spinal cord
Polgár, E., Fowler, J. H., McGill, M. M., & Todd, A. J. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01500-0 · Cited by 194 · see citing works
Self-citationHeinke, B., Ruscheweyh, R., Forsthuber, L., Wunderbaldinger, G., & Sandkühler, J. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.070540 · Cited by 194 · see citing works
No NO, no pain? The role of nitric oxide and cGMP in spinal pain processing
Schmidtko, A., Tegeder, I., & Geißlinger, G. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2009.01.010 · Cited by 187 · see citing works
Neuropeptides as synaptic transmitters
Salio, C., Lossi, L., Ferrini, F., & Merighi, A. (2006) · Cell and Tissue Research · doi:10.1007/s00441-006-0268-3 · Cited by 181 · see citing works
Abe, T., Matsumura, S., Katano, T., Mabuchi, T., Takagi, K., Xu, L., Yamamoto, A., Hattori, K., Yagi, T., Watanabe, M., et al. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04340.x · Cited by 170 · see citing works
Costorage and coexistence of neuropeptides in the mammalian CNS
Merighi, A. (2002) · Progress in Neurobiology · doi:10.1016/s0301-0082(01)00031-4 · Cited by 158 · 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
Todd, A. J., SPIKE, R. C., & Polgár, E. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00669-6 · Cited by 147 · see citing works
Self-citationBoyle, K. A., Gradwell, M. A., Yasaka, T., Dickie, A. C., Polgár, E., Ganley, R. P., Orr, D. P. H., Watanabe, M., Abraira, V. E., Kuehn, E. D., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.06.040 · Cited by 131 · see citing works
Mabuchi, T., Shintani, N., Matsumura, S., Okuda‐Ashitaka, E., Hashimoto, H., Muratani, T., Minami, T., Baba, A., & Ito, S. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0983-04.2004 · Cited by 127 · see citing works
Histochemistry of nitric oxide synthase in the nervous system.
Blottner, D., Grozdanovic, Z., & Gossrau, R. (1995) · PubMed · Cited by 127 · 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
Self-citationA Quantitative Study of Inhibitory Interneurons in Laminae I-III of the Mouse Spinal Dorsal Horn
Polgár, E., Durrieux, C., Hughes, D. I., & Todd, A. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078309 · Cited by 123 · see citing works
Self-citationMartin, W. J., Liu, H., Wang, H., Malmberg, A. B., & Basbaum, A. I. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00314-5 · Cited by 116 · see citing works
Muscarinic facilitation of GABA release in substantia gelatinosa of the rat spinal dorsal horn
Baba, H., Kohno, T., Okamoto, M., Goldstein, P. A., Shimoji, K., & Yoshimura, M. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.083br.x · Cited by 115 · 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
Self-citationHistochemistry of nitric oxide synthase in the nervous system
Blottner, D., Grozdanovic, Z., & Gossrau, R. (1995) · The Histochemical Journal · doi:10.1007/bf02388304 · Cited by 107 · see citing works
Kerr, R., Maxwell, & Todd (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00048.x · Cited by 106 · see citing works
Neuroanatomical substrates of spinal nociception
Todd, A. J., & Koerber, H. R. (2006) · Elsevier eBooks · doi:10.1016/b0-443-07287-6/50009-6 · Cited by 100 · see citing works
Self-citationMabuchi, T., Matsumura, S., Okuda‐Ashitaka, E., Kitano, T., Kojima, H., Nagano, T., Minami, T., & Ito, S. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02575.x · Cited by 98 · 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
Self-citationAlbuquerque, C., Lee, C. J., Jackson, A. C., & MacDermott, A. B. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00691.x · Cited by 95 · see citing works
Some inhibitory neurons in the spinal cord develop c-fos-immunoreactivity after noxious stimulation
Todd, A. J., SPIKE, R. C., Brodbelt, A. R., Price, R. F., & Shehab, S. A. S. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90525-8 · Cited by 94 · see citing works
Self-citationPolgár, E., Sardella, T. C. P., Tiong, S. Y. X., Locke, S., Watanabe, M., & Todd, A. J. (2013) · Pain · doi:10.1016/j.pain.2013.05.001 · Cited by 93 · see citing works
Self-citationJinno, S., & Kosaka, T. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10251 · Cited by 90 · see citing works
Kemp, T., SPIKE, R. C., Watt, C., & Todd, A. J. (1996) · Neuroscience · doi:10.1016/0306-4522(96)00333-8 · Cited by 90 · see citing works
Self-citationCentral Nervous System Targets: Inhibitory Interneurons in the Spinal Cord
Hughes, D. I., & Todd, A. J. (2020) · Neurotherapeutics · doi:10.1007/s13311-020-00936-0 · Cited by 88 · see citing works
Self-citationMechanisms of orofacial pain control in the central nervous system
Takemura, M., Sugiyo, S., Moritani, M., Kobayashi, M., & Yonehara, N. (2006) · Archivum histologicum japonicum · doi:10.1679/aohc.69.79 · Cited by 88 · see citing works
Graham, B. A., Brichta, A. M., & Callister, R. J. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.072645 · Cited by 82 · see citing works
Brumovsky, P. R., Stanić, D., Shuster, S. J., Herzog, H., Villar, M. J., & Hökfelt, T. G. M. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20639 · Cited by 77 · see citing works
Loomis, C. W., Khandwala, H., Osmond, G., & Hefferan, M. P. (2001) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)38813-5 · Cited by 76 · see citing works
Inflammation alters cation chloride cotransporter expression in sensory neurons
Morales‐Aza, B. M., Chillingworth, N. L., Payne, J. A., & Donaldson, L. F. (2004) · Neurobiology of Disease · doi:10.1016/j.nbd.2004.05.010 · Cited by 76 · see citing works
Dynorphin is Expressed Primarily by GABAergic Neurons That Contain Galanin in the Rat Dorsal Horn
Sardella, T. C. P., Polgár, E., Garzo, F., Furuta, T., Kaneko, T., Watanabe, M., & Todd, A. J. (2011) · Molecular Pain · doi:10.1186/1744-8069-7-76 · Cited by 76 · see citing works
Self-citationGalanin is contained in GABAergic neurons in the rat spinal dorsal horn
Simmons, D. R., SPIKE, R. C., & Todd, A. J. (1995) · Neuroscience Letters · doi:10.1016/0304-3940(95)11358-4 · Cited by 72 · see citing works
Self-citationMesnage, B., Gaillard, S., Godin, A. G., Rodeau, J., Hammer, M., Von Engelhardt, J., Wiseman, P. W., De Koninck, Y., Schlichter, R., & Cordero‐Erausquin, M. (2011) · Journal of Comparative Neurology · doi:10.1002/cne.22668 · Cited by 71 · see citing works
Quantitative study of NPY‐expressing GABAergic neurons and axons in rat spinal dorsal horn
Polgár, E., Sardella, T. C. P., Watanabe, M., & Todd, A. J. (2010) · The Journal of Comparative Neurology · doi:10.1002/cne.22570 · Cited by 71 · see citing works
Self-citationNeurotrophins in spinal cord nociceptive pathways
Merighi, A., Carmignoto, G., Gobbo, S., Lossi, L., Salio, C., Vergnano, A. M., & Zonta, M. (2004) · Progress in brain research · doi:10.1016/s0079-6123(03)46019-6 · Cited by 65 · see citing works
Nicotinic cholinergic receptors: potential targets for inflammatory pain relief
Lawand, N., Lu, Y. C., & Westlund, K. N. (1999) · Pain · doi:10.1016/s0304-3959(98)00221-8 · Cited by 64 · see citing works
Tiong, S. Y., Polgár, E., van Kralingen, J. C., Watanabe, M., & Todd, A. J. (2011) · Molecular Pain · doi:10.1186/1744-8069-7-36 · Cited by 62 · see citing works
Self-citationAimar, P., Pasti, L., Carmignoto, G., & Merighi, A. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-24-10375.1998 · Cited by 62 · see citing works
Braz, J. M., & Basbaum, A. I. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.07.051 · Cited by 59 · see citing works
Subcellular distribution of histamine, GABA and galanin in tuberomamillary neurons in vitro
Kukko‐Lukjanov, T., & Panula, P. (2003) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(03)00043-7 · Cited by 59 · see citing works
Inhibitory Coupling between Inhibitory Interneurons in the Spinal Cord Dorsal Horn
Labrakakis, C., Lorenzo, L.-É., Bories, C., Ribeiro‐da‐Silva, A., & Koninck, Y. D. (2009) · Molecular Pain · doi:10.1186/1744-8069-5-24 · Cited by 56 · see citing works
Gamboa-Esteves, F. O., Kaye, J. C., McWilliam, P. N., Lima, D., & Batten, T. F. C. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00071-9 · Cited by 56 · see citing works
Sardella, T. C. P., Polgár, E., Watanabe, M., & Todd, A. J. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.07.011 · Cited by 55 · see citing works
Self-citationHCN4 subunit expression in fast-spiking interneurons of the rat spinal cord and hippocampus
Hughes, D. I., Boyle, K. A., Kinnon, C. M., Bilsland, C., Quayle, J. A., Callister, R. J., & Graham, B. A. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.01.028 · Cited by 55 · 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
Conte, D., Legg, E. D., McCourt, A. C., Silajdžić, E., Nagy, G., & Maxwell, D. J. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.02.013 · Cited by 51 · 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
Merighi, A. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.06.012 · Cited by 50 · see citing works
Song, B., & Marvizón, J. C. G. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-27-09171.2003 · Cited by 50 · see citing works
Hughes, A. S., Averill, S., King, V. R., Molander, C., & Shortland, P. J. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.01.082 · Cited by 45 · see citing works
Wu, S., Wang, W., Li, H., Wang, Y., Feng, Y., & Li, Y.-Q. (2010) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2010.01.005 · Cited by 44 · 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
Self-citationCassam, A. K., Llewellyn‐Smith, I. J., & Weaver, L. C. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00599-4 · Cited by 44 · see citing works
Inhibitory effect of nitric oxide on neuronal activity in the periaqueductal grey matter of the rat
Lovick, T. A., & Key, B. J. (1996) · Experimental Brain Research · doi:10.1007/bf00227261 · Cited by 44 · see citing works
Tatsumi, S., Mabuchi, T., Abe, T., Xu, L., Minami, T., & Ito, S. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.08.043 · Cited by 41 · see citing works
Diversity of inhibitory and excitatory parvalbumin interneuron circuits in the dorsal horn
Gradwell, M. A., Boyle, K. A., Browne, T. J., Bell, A. M., Leonardo, J., Reyes, F. S. P., Dickie, A. C., Smith, K. M., Callister, R. J., Dayas, C. V., et al. (2021) · Pain · doi:10.1097/j.pain.0000000000002422 · Cited by 39 · see citing works
Dougherty, K. J., Sawchuk, M. A., & Hochman, S. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.06.055 · Cited by 35 · see citing works
Nitric Oxide-Mediated Pain Processing in the Spinal Cord
Schmidtko, A. (2015) · Handbook of experimental pharmacology · doi:10.1007/978-3-662-46450-2_6 · Cited by 35 · see citing works
Wiley, R. G., Lemons, L. L., & Kline, R. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.12.017 · Cited by 34 · see citing works
Dun, N. J., Dun, S. L., Hwang, L.-L., & Förstermann, U. (1995) · Neuroscience Letters · doi:10.1016/0304-3940(95)11582-h · Cited by 34 · see citing works
Buritova, J., Chapman, V., Honoré, P., & Besson, J. (1996) · Neuroscience · doi:10.1016/0306-4522(96)00071-1 · Cited by 32 · see citing works
Iwagaki, N., Garzillo, F., Polgár, E., Riddell, J. S., & Todd, A. J. (2013) · Molecular Pain · doi:10.1186/1744-8069-9-56 · Cited by 31 · see citing works
Self-citationVles, J. S. H., de Louw, A. J. A., Steinbusch, H. W. M., Ittersum, M. M., Steinbusch, H. W. M., Blanco, C. E., Axer, H., Troost, J., & de Vente, J. (2000) · Brain Research · doi:10.1016/s0006-8993(99)02434-8 · Cited by 31 · see citing works
Stewart, W. B., Jr., & Maxwell, D. J. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00116-7 · Cited by 30 · see citing works
Grinspan, J. B., Reeves, M. F., Coulaloglou, M. J., Nathanson, D. R., & Pleasure, D. (1996) · Journal of Neuroscience Research · doi:10.1002/(sici)1097-4547(19961115)46:4 · Cited by 60 · see citing works
Ichikawa, H., & Helke, C. J. (1996) · Brain Research · doi:10.1016/0006-8993(96)00798-6 · Cited by 30 · see citing works
Role of Nitric Oxide on the Blood–Brain and Spinal Cord Barriers
Sharma, H. S., & Alm, P. (2004) · Elsevier eBooks · doi:10.1016/b978-012639011-7/50018-8 · Cited by 29 · see citing works
Labrakakis, C., Rudolph, U., & Koninck, Y. D. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00424 · Cited by 28 · see citing works
Hossaini, M., Duraku, L. S., Kohli, S. K., Jongen, J. L. M., & Holstege, J. C. (2013) · Brain Research · doi:10.1016/j.brainres.2013.10.044 · Cited by 28 · see citing works
García‐Magro, N., Negredo, P., Martín, Y. B., Núñez, Á., & Avendaño, C. (2020) · The Journal of Headache and Pain · doi:10.1186/s10194-020-01161-y · Cited by 28 · see citing works
Bertini, G., Peng, Z.-C., & Bentivoglio, M. (1996) · Brain Research Bulletin · doi:10.1016/0361-9230(95)02133-7 · Cited by 28 · see citing works
Cao, J., Ding, H., He, J., Zhang, L., Shi-ming, D., & Yin-ming, Z. (2005) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2005.01.009 · Cited by 26 · see citing works
Sasaki, A., Mabuchi, T., Serizawa, K., Takasaki, I., Andoh, T., Shiraki, K., Ito, S., & Kuraishi, Y. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.09.067 · Cited by 26 · see citing works
Cummings, S. L., Truong, B. G., & Gietzen, D. W. (1998) · Peptides · doi:10.1016/s0196-9781(97)00468-3 · Cited by 25 · see citing works
Milner, T. A., Okada, J., & Pickel, V. M. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903530307 · Cited by 25 · see citing works
Transcriptional profile of spinal dynorphin-lineage interneurons in the developing mouse
Serafin, E. K., Chamessian, A., Li, J., Zhang, X., McGann, A., Brewer, C. L., Berta, T., & Baccei, M. (2019) · Pain · doi:10.1097/j.pain.0000000000001636 · Cited by 24 · see citing works
Barreiro‐Iglesias, A., Anadón, R., & Rodicio, M. C. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.02.030 · Cited by 22 · see citing works
Jinno, S., Kinukawa, N., & Kosaka, T. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02292-2 · Cited by 23 · see citing works
Dieb, W., & Hafidi, A. (2014) · European Journal of Pain · doi:10.1002/ejp.525 · Cited by 22 · see citing works
A Trigeminoreticular Pathway: Implications in Pain
Panneton, W. M., Gan, Q., & Livergood, R. S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024499 · Cited by 22 · see citing works
Genes linked to species diversity in a sexually dimorphic communication signal in electric fish
Smith, G. T., Proffitt, M. R., Smith, A. R., & Rusch, D. B. (2017) · Journal of Comparative Physiology A · doi:10.1007/s00359-017-1223-3 · Cited by 23 · see citing works
Tong, C., Kaftan, E. J., & MacDermott, A. B. (2008) · Molecular Pain · doi:10.1186/1744-8069-4-44 · Cited by 20 · see citing works
Serafin, E. K., Paranjpe, A., Brewer, C. L., & Baccei, M. L. (2020) · Pain · doi:10.1097/j.pain.0000000000002007 · Cited by 19 · see citing works
Rho-kinase mediates spinal nitric oxide formation by prostaglandin E2 via EP3 subtype
Matsumura, S., Abe, T., Mabuchi, T., Katano, T., Takagi, K., Okuda‐Ashitaka, E., Tatsumi, S., Nakai, Y., Hidaka, H., Suzuki, M., et al. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.09.058 · Cited by 19 · see citing works
Takemura, M., Tsujio, A., Iwase, K., Shimada, T., & Shigenaga, Y. (1998) · Brain Research · doi:10.1016/s0006-8993(97)01210-9 · Cited by 18 · see citing works
Larsson, M. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1566-0 · Cited by 17 · see citing works
The distribution and characterization of NADPH-d/NOS-IR neurons in the rat cuneate nucleus
Wang, T., Lue, J., Shieh, J.-Y., & Wen, C.-Y. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02403-9 · Cited by 17 · see citing works
Properties of spinal lamina III GABAergic neurons in naïve and in neuropathic mice
Gassner, M., Leitner, J., Gruber-Schoffnegger, D., Forsthuber, L., & Sandkühler, J. (2013) · European Journal of Pain · doi:10.1002/j.1532-2149.2013.00294.x · Cited by 16 · see citing works
- Authors
- Laing, I., Todd, A. J., Heizmann, C. W., & Schmidt, H. H. H. W.
- Affiliations
- University of Glasgow (GB)
- University of Zurich (CH)
- Universitätsklinikum Würzburg (DE)
- Corresponding author
- Todd, A.J.
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 1994-07
- Volume
- 61
- Issue
- 1
- Pages
- 123-132
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W2029706214
- Cited by
- 177
- References
- 55
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 3 · 2023: 4 · 2022: 2 · 2021: 9 · 2020: 8 · 2019: 4 · 2018: 5 · 2017: 9 · 2016: 3 · 2015: 5 · 2014: 4 · 2013: 10 · 2012: 1
- FWCI
- 4.76
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust
- Topics
- Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- GABAergic neurons, dorsal horn, parvalbumin, nitric oxide synthase, NADPH-diaphorase, neuropeptide Y, enkephalin, acetylcholine, glycine, neuropeptide co-localization, inhibitory interneurons, cholinergic neurons, rats
- MeSH terms
- Acetylcholine, Amino Acid Oxidoreductases, Animals, Enkephalins, Female, gamma-Aminobutyric Acid, Glycine, Immunohistochemistry, Male, NADPH Dehydrogenase, Neurons, Neuropeptide Y, Neuropeptides, Parvalbumins, Spinal Cord, Biomarkers, Rats, Sprague-Dawley, Neurotransmitter Agents, Nitric Oxide Synthase, Mice, Rats
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