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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 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]
Citations
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
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
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 1,675
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
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 1,329
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
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
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
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
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
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
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
Self-citationTodd, A. J., & Sullivan, A. C. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902960312 · Cited by 501
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
Intracellular 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 451
Self-citationKosaka, T., Tauchi, M., & Dahl, J. L. (1988) · Experimental Brain Research · doi:10.1007/bf00247609 · Cited by 417
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
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 363
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
Todd, A. J., & SPIKE, R. C. (1993) · Progress in Neurobiology · doi:10.1016/0301-0082(93)90045-t · Cited by 330
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
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
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
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
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
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
Self-citationThomas, E., & Pearse, A. G. E. (1964) · Acta Neuropathologica · doi:10.1007/bf00684399 · Cited by 227
Blottner, D., & Baumgarten, H. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903160105 · Cited by 222
Anderson, C. R. (1992) · Neuroscience Letters · doi:10.1016/0304-3940(92)90571-n · Cited by 204
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
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
Self-citationAntal, M., Freund, T. F., & Polgár, E. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902950310 · Cited by 156
Kosaka, T., & Heizmann, C. W. (1989) · Brain Research · doi:10.1016/0006-8993(89)90048-6 · Cited by 153
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
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
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
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 140
Self-citationRibeiro‐da‐Silva, A., & Cuello, A. C. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902950303 · Cited by 135
Rowan, S., Todd, A. J., & SPIKE, R. C. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90218-5 · Cited by 112
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
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
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
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
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
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
Todd, A. J. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90093-4 · Cited by 79
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 79
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
Todd, A., Spike, R., Price, R. F., & Neilson, M. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-02-00774.1994 · Cited by 64
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
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
Self-citationTodd, A. J., Russell, G., & SPIKE, R. C. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90176-3 · Cited by 48
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
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
Self-citationDoyle, C. A., & Maxwell, D. J. (1993) · Brain Research · doi:10.1016/0006-8993(93)91315-j · Cited by 23
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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
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Metadata
- 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 (medical) › 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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