A population of large neurons in laminae III and IV of the rat spinal cord that have long dorsal dendrites and lack the neurokinin 1 receptor

European Journal of Neuroscience

Volumn 26, Issue 6, 2007, Pages 1587-1598

  Polgár, Erika ^a   Thomson, Suzanne ^a   Maxwell, David J ^a   Al Khater, Khulood ^a   Todd, Andrew J ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Confocal microscopy; NF200; NK1 receptor; Projection neuron

Indexed keywords

NEUROKININ 1 RECEPTOR; SUBSTANCE P; TRACER;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL POPULATION; CONTROLLED STUDY; DENDRITIC SPINE; IMMUNOHISTOCHEMISTRY; LAMINA PROPRIA; MEDULLA OBLONGATA; NERVE FIBER MEMBRANE; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL CORD DORSAL HORN; SPINAL CORD NERVE CELL; SPINOTHALAMIC TRACT;

ANIMALS; AXONS; DENDRITES; IMMUNOHISTOCHEMISTRY; MALE; MEDULLA OBLONGATA; MICROSCOPY, CONFOCAL; NEUROFILAMENT PROTEINS; NEURONS; NEURONS, AFFERENT; RATS; RATS, WISTAR; RECEPTORS, NEUROKININ-1; SPINAL CORD; STILBAMIDINES; SUBSTANCE P; THALAMUS;

EID: 34548676561     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05793.x     Document Type: Article

References (44)

1. Bleazard, L., Hill, R.G. Morris, R. (1994) The correlation between the distribution of the NK1 receptor and the actions of tachykinin agonists in the dorsal horn of the rat indicates that substance P does not have a functional role on substantia gelatinosa (lamina II) neurons. JNeurosci., 14, 7655 7664.
2. Brown, A.G. (1981) Organization in the Spinal Cord: the Anatomy and Physiology of Identified Neurones. Springer, Berlin.
3. Brown, A.G. Fyffe, R.E. (1981) Form and function of dorsal horn neurones with axons ascending the dorsal columns in cat. JPhysiol., 321, 31 47.
4. Brown, J.L., Liu, H., Maggio, J.E., Vigna, S.R., Mantyh, P.W. Basbaum, A.I. (1995) Morphological characterization of substance P receptor- immunoreactive neurons in the rat spinal cord and trigeminal nucleus caudalis. JComp. Neurol., 356, 327 344.
5. Cuello, A.C., Galfre, G. Milstein, C. (1979) Detection of substance P in the central nervous system by a monoclonal antibody. Proc. Natl Acad. Sci. USA, 76, 3532 3536.
6. Gauriau, C. Bernard, J.F. (2004) A comparative reappraisal of projections from the superficial laminae of the dorsal horn in the rat: the forebrain. JComp. Neurol., 468, 24 56.
7. Gerke, M.B. Plenderleith, M.B. (2004) Ultrastructural analysis of the central terminals of primary sensory neurones labelled by transganglionic transport of bandeiraea simplicifolia I-isolectin B4. Neuroscience, 127, 165 175.
8. Giesler, G.J. Jr., Nahin, R.L. Madsen, A.M. (1984) Postsynaptic dorsal column pathway of the rat. I. Anatomical studies. JNeurophysiol., 51, 260 275.
9. Guo, A., Vulchanova, L., Wang, J., Li, X. Elde, R. (1999) Immunocytochemical localization of the vanilloid receptor 1 (VR1): relationship to neuropeptides, the P2X3 purinoceptor and IB4 binding sites. Eur. J. Neurosci., 11, 946 958.
10. Hokfelt, T., Kellerth, J.O., Nilsson, G. Pernow, B. (1975) Substance P: localization in the central nervous system and in some primary sensory neurons. Science, 190, 889 890.
11. Ju, G., Hokfelt, T., Brodin, E., Fahrenkrug, J., Fischer, J.A., Frey, P., Elde, R.P. Brown, J.C. (1987) Primary sensory neurons of the rat showing calcitonin gene-related peptide immunoreactivity and their relation to substance P-, somatostatin-, galanin-, vasoactive intestinal polypeptide- and cholecystokinin-immunoreactive ganglion cells. Cell Tissue Res., 247, 417 431.
12. Lawson, S.N., Crepps, B.A. Perl, E.R. (1997) Relationship of substance P to afferent characteristics of dorsal root ganglion neurones in guinea-pig. JPhysiol., 505, 177 191.
13. Lima, D., Mendes-Ribeiro, J.A. Coimbra, A. (1991) The spino-latero-reticular system of the rat: projections from the superficial dorsal horn and structural characterization of marginal neurons involved. Neuroscience, 45, 137 152.
14. Littlewood, N.K., Todd, A.J., Spike, R.C., Watt, C. Shehab, S.A. (1995) The types of neuron in spinal dorsal horn which possess neurokinin-1 receptors. Neuroscience, 66, 597 608.
15. Llewellyn-Smith, I.J. Minson, J.B. (1992) Complete penetration of antibodies into vibratome sections after glutaraldehyde fixation and ethanol treatment: light and electron microscopy for neuropeptides. JHistochem. Cytochem., 40, 1741 1749.
16. Mantyh, P.W., DeMaster, E., Malhotra, A., Ghilardi, J.R., Rogers, S.D., Mantyh, C.R., Liu, H., Basbaum, A.I., Vigna, S.R., Maggio, J.E. Simone, D.A. (1995) Receptor endocytosis and dendrite reshaping in spinal neurons after somatosensory stimulation. Science, 268, 1629 1632.
17. Marshall, G.E., Shehab, S.A.S., Spike, R.C. Todd, A.J. (1996) Neurokinin-1 receptors on lumbar spinothalamic neurons in the rat. Neuroscience, 72, 255 263.
18. McLeod, A.L., Krause, J.E. Ribeiro-Da-Silva, A. (2000) Immunocytochemical localization of neurokinin B in the rat spinal dorsal horn and its association with substance P and GABA: an electron microscopic study. JComp. Neurol., 420, 349 362.
19. Michael, G.J. Priestley, J.V. (1999) Differential expression of the mRNA for the vanilloid receptor subtype 1 in cells of the adult rat dorsal root and nodose ganglia and its downregulation by axotomy. JNeurosci., 19, 1844 1854.
20. Molander, C., Xu, Q. Grant, G. (1984) The cytoarchitectonic organization of the spinal cord in the rat. I. The lower thoracic and lumbosacral cord. JComp. Neurol., 230, 133 141.
21. Naim, M., Spike, R.C., Watt, C., Shehab, S.A. Todd, A.J. (1997) Cells in laminae III and IV of the rat spinal cord that possess the neurokinin-1 receptor and have dorsally directed dendrites receive a major synaptic input from tachykinin-containing primary afferents. JNeurosci., 17, 5536 5548.
22. Nakaya, Y., Kaneko, T., Shigemoto, R., Nakanishi, S. Mizuno, N. (1994) Immunohistochemical localization of substance P receptor in the central nervous system of the adult rat. JComp. Neurol., 347, 249 274.
23. Palecek, J., Paleckova, V. Willis, W.D. (2003) Postsynaptic dorsal column neurons express NK1 receptors following colon inflammation. Neuroscience, 116, 565 572.
24. Paxinos, G. Watson, C. (1997) The Rat Brain in Stereotaxic Coordinates, 3rd Edn. Academic Press, San Diego.
25. Polgar, E., Campbell, A.D., MacIntyre, L.M., Watanabe, M. Todd, A.J. (2007) Phosphorylation of ERK in neurokinin 1 receptor-expressing neurons in laminae III and IV of the rat spinal dorsal horn following noxious stimulation. Mol. Pain, 3, 4.
26. Polgár, E., Furuta, T., Kaneko, T. Todd, A.J. (2006) Characterization of neurons that express preprotachykinin B in the dorsal horn of the rat spinal cord. Neuroscience, 139, 687 697.
27. Polgár, E., Shehab, S.A.S., Watt, C. Todd, A.J. (1999) GABAergic neurons that contain neuropeptide Y selectively target cells with the neurokinin 1 receptor in laminae III and IV of the rat spinal cord. JNeurosci., 19, 2637 2646.
28. Ramon y Cajal, S. (1909) Histologie Du Système Nerveux de L'homme et Des Vertébrés, I. Maloine, Paris.
29. Réthelyi, M. Szentágothai, J. (1969) The large synaptic complexes of the substantia gelatinosa. Exp. Brain Res., 7, 258 274.
30. Rexed, B. (1952) The cytoarchitectonic organization of the spinal cord in the cat. JComp. Neurol., 96, 414 495.
31. Ribeiro-da-Silva, A., Castro-Lopes, J.M. Coimbra, A. (1986) Distribution of glomeruli with fluoride-resistant acid phosphatase (FRAP)-containing terminals in the substantia gelatinosa of the rat. Brain Res., 377, 323 329.
32. Ribeiro-da-Silva, A. Coimbra, A. (1982) Two types of synaptic glomeruli and their distribution in laminae I-III of the rat spinal cord. JComp. Neurol., 209, 176 186.
33. Sakamoto, H., Spike, R.C. Todd, A.J. (1999) Neurons in laminae III and IV of the rat spinal cord with the neurokinin-1 receptor receive few contacts from unmyelinated primary afferents which do not contain substance P. Neuroscience, 94, 903 908.
34. Scheibel, M.E. Scheibel, A.B. (1966) Terminal axonal patterns in cat spinal cord. I. The lateral corticospinal tract. Brain Res., 2, 333 350.
35. Schoenen, J. (1982) The dendritic organization of the human spinal cord: the dorsal horn. Neuroscience, 7, 2057 2087.
36. Silverman, J.D. Kruger, L. (1990) Selective neuronal glycoconjugate expression in sensory and autonomic ganglia: relation of lectin reactivity to peptide and enzyme markers. JNeurocytol., 19, 789 801.
37. Spike, R.C., Puskar, Z., Sakamoto, H., Stewart, W., Watt, C. Todd, A.J. (2002) MOR-1-immunoreactive neurons in the dorsal horn of the rat spinal cord: evidence for nonsynaptic innervation by substance P-containing primary afferents and for selective activation by noxious thermal stimuli. Eur. J. Neurosci., 15, 1306 1316.
38. Stucky, C.L. Lewin, G.R. (1999) Isolectin B(4)-positive and -negative nociceptors are functionally distinct. JNeurosci., 19, 6497 6505.
39. Szentágothai, J. (1964) Neuronal and synaptic arrangement in the substantia gelatinosa Rolandi. JComp. Neurol., 122, 219 239.
40. Todd, A.J. (1989) Cells in laminae III and IV of rat spinal dorsal horn receive monosynaptic primary afferent input in lamina II. JComp. Neurol., 289, 676 686.
41. Todd, A.J. Koerber, H.R. (2005) Neuroanatomical substrates of spinal nociception. In McMahon, S. Koltzenburg, M. (Eds), Wall and Melzack's Textbook of Pain, 5th Edn. Elsevier, Edinburgh, pp. 73 90.
42. Todd, A.J., McGill, M.M. Shehab, S.A. (2000) Neurokinin 1 receptor expression by neurons in laminae I, III and IV of the rat spinal dorsal horn that project to the brainstem. Eur. J. Neurosci., 12, 689 700.
43. Wang, H., Rivero-Melian, C., Robertson, B. Grant, G. (1994) Transganglionic transport and binding of the isolectin B4 from Griffonia simplicifolia I in rat primary sensory neurons. Neuroscience, 62, 539 551.
44. Willis, W.D. Coggeshall, R.E. (2004) Sensory Mechanisms of the Spinal Cord, Vol. 2: Ascending Sensory Tracts and Their Descending Control, 3rd Edn. Kluwer Academic, New York.