Skip to main content
NCBI home page
Cellular and Molecular Neurobiology logoLink to Cellular and Molecular Neurobiology
. 1996 Nov;16(6):625–648. doi: 10.1007/BF02151901

Tyrosine hydroxylase-containing neurons in the spinal cord of the chicken. I. Development and analysis of catecholamine synthesis capabilities

James A Wallace 1,✉, Audrey A Romero 1, Anna M Gabaldon 1, Victoria A Roe 1, Sandra L Saavedra 1, Jerinda Lobner 1
PMCID: PMC11563113  PMID: 9013027

Abstract

  1. The development of tyrosine hydroxylase-immunoreactive (TH-IR) neurons was examined in the spinal cord of the chick embryo and hatchling.

  2. Two groups of TH-IR cells are described, both of which appear to reach their full complement in number relatively late in embryonic development. One group is comprised of numerous cells located ventral to the central canal which make direct contact with the lumen of the canal. The other group consists of large multipolar neurons that reside in the dorsal horn, more commonly along the outer margin of the gray matter within lamina I and II, and less frequently deeper in the dorsal horn within medial portions of laminae V, VI or VII.

  3. TH-IR cells ventral to the central canal in the chick are comparable in location to dopamine (DA)-containing spinal cord cells in lower vertebrate species. In contrast, the dorsally-suited TH-IR cells in the chick are known only to occur in similar positions in higher vertebrates. Therefore, the chick is novel in that the presence ofboth groups of TH-IR cells appearing together in significant numbers within the spinal cord has not been shown in any other species studied to date.

  4. The TH-containing cells in the chick cord do not appear to contain the catecholamine biosynthesis enzymes, DBH or PNMT. Moreover, using anti-DA immunocytochemistry, neither group of TH-IR cells demonstrated detectable levels of DA in control animals nor in animals pretreated with inhibitors of MAO (MAO-I).

  5. However, a difference was noted though between the two TH-IR cell groups in terms of their responses to exogenously supplied L-DOPA, the immediate precursor to DA. With the administration of L-DOPA and a MAO-I to chick hatchlings, cells in the region ventral to the central canal stained intensely for DA. In contrast, the same treatment failed to produce DA-immunoreactive cells in the dorsal horn.

  6. One reasonable hypothesis for these results is that the TH-IR cells ventral to the central canal contain an active form of AADC, the enzyme that converts L-DOPA to DA. With this interpretation, if these cells can produce DA from L-DOPA, yet do not appear to synthesize DA endogenously, it would appear that the TH enzyme contained in these cells occurs in aninactive form. Whether the TH enzyme in the dorsally located immunoreactive cells is also inactive is uncertain since it remains unclear whether they contain AADC.

Key Words: tyrosine hydroxylase immunocytochemistry, spinal cord, chick embryo, dopamine immunocytochemistry, evolution, CSF-contacting neurons

References

  1. Baumgarten, H. G. (1972). Biogenic monoamines in the cyclostome and lower vertebrate brain.Prog. Histochem. Cytochem.4:1–90. [DOI] [PubMed] [Google Scholar]
  2. Baumgarten, H. G., Falck, B., and Wartenberg, H. (1970). Adrenergic neurons in the spinal cord of the pike (Esox lucius) and their relation to the caudal neurosecretory system.Z. Zellforsch.107:479–498. [DOI] [PubMed] [Google Scholar]
  3. Carlsson, A., Falck, B., Fuxe, K. and Hillarp, N. Å. (1964). Cellular localization of monoamines in the spinal cord.Acta Physiol. Scand.60:112–119. [DOI] [PubMed] [Google Scholar]
  4. Caserta, M., and Ross, L. L. (1978). Biochemical and morphological studies of synaptogenesis in the avian sympathetic cell column.Brain Res.144:241–255. [DOI] [PubMed] [Google Scholar]
  5. Chesler, M., and Nicholson, C. (1985). Organization of the filum terminale in the frog.J. Comp. Neurol.239:431–444. [DOI] [PubMed] [Google Scholar]
  6. Dahlström, A., and Fuxe, K. (1964). Evidence for the existence of monoamine neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brain stem neurons.Acta Physiol. Scand.62:Suppl. 232. [PubMed] [Google Scholar]
  7. Dahlström, A., and Fuxe, K. (1965). Evidence for the existence of monoamine neurons in the central nervous system. II. Experimentally induced changes in the intraneuronal amine levels of bulbospinal neuron systems.Acta Physiol. Scand.64:Suppl. 247. [PubMed] [Google Scholar]
  8. Dietl, M., Arluison, M., Mouchet, P., Feuerstein, C., Manier, M., and Thibault, J. (1985). Immunohistochemical demonstration of catecholaminergic cell bodies in the spinal cord of the rat.Histochemistry82:385–389. [DOI] [PubMed] [Google Scholar]
  9. Du, F., and Dubois, P. (1988a). Distribution of substance P and vasoactive intestinal polypeptide neurons in the chicken spinal cord, with notes on their postnatal development.J. Comp. Neurol.278:253–264. [DOI] [PubMed] [Google Scholar]
  10. Du, F., and Dubois, P. (1988b). Development and distribution of enkephalin-immunoreactive elements in the chicken spinal cord.Neuroscience27:251–266. [DOI] [PubMed] [Google Scholar]
  11. Dubé, L., and Parent, A. (1981). The monoamine-containing neurons in avian brain. I. A study of the brain stem of the chicken (Gallus domesticus) by means of fluorescence and acetylcholinestrase histochemistry.J. Comp. Neurol.196:695–708. [DOI] [PubMed] [Google Scholar]
  12. Franzoni, M. F., Thibault, J., Fasolo, A., Martinoli, M. G., Scaranari, F., and Calas, A. (1986). Organization of tyrosine-hydroxylase immunopositive neurons in the brain of the crested newt,Triturus cristatus carnifex.J. Comp. Neurol.251:121–134. [DOI] [PubMed] [Google Scholar]
  13. Geffard, M., Buijs, R. M., Seguela, P., Pool, C. W., and La Moal, M. (1984). First demonstration of highly specific and sensitive antibodies against dopamine.Brain Res.294:161–165. [DOI] [PubMed] [Google Scholar]
  14. Gonzalez, A., and Smeets, W. J. A. J. (1991). Comparative analysis of dopamine and tyrosine hydroxylase immunoreactivities in the brain of two amphibians, the anuranRana ridibunda and the urodelePleurodeles waltlii.J. Comp. Neurol.303:457–477. [DOI] [PubMed] [Google Scholar]
  15. Gonzalez, A., Tuinhof, R., and Smeets, W. J. A. J. (1993). Distribution of tyrosine hydroxylase and dopamine immunoreactivities in the brain of the South America clawed frogXenopus laevis.Anat. Embryol.187:193–201. [DOI] [PubMed] [Google Scholar]
  16. Guglielmone, R., and Panzica, G. C. (1985). Early appearance of catecholaminergic neurons in the central nervous system of precocial and altricial avian species.Cell Tissue Res.240:381–384. [DOI] [PubMed] [Google Scholar]
  17. Hamburger, V., and Hamilton, H. L. (1951). A series of normal stages in the development of the chick embryo.J. Morphol.88:49–92. [PubMed] [Google Scholar]
  18. Harrington, C. A., Lewis, E. J., Krzemien, D., and Chikaraishi, D. M. (1987). Identification and cell type specificity of the tyrosine hydroxylase gene promoter.Nucleic Acids Res.15:2363–2384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Heathcote, R. D., and Chen, A. (1993). A nonrandom interneuronal pattern in the developing frog spinal cord.J. Comp. Neurol.328:437–448. [DOI] [PubMed] [Google Scholar]
  20. Heathcote, R. D., and Chen, A. (1994). Morphogenesis of catecholaminergic interneurons in the frog spinal cord.J. Comp. Neurol.342:57–68. [DOI] [PubMed] [Google Scholar]
  21. Honma, S. (1970). Presence of monoaminergic neurons in the spinal cord and intestine of the lampreyLampetra japonica.Arch. Histol. Jpn.32:383–393. [DOI] [PubMed] [Google Scholar]
  22. Ikeda, H., and Gotoh, J. (1971). Distribution of monoamine-containing cells in the central nervous system of the chicken.Japan J. Pharmacol.21:763–784. [DOI] [PubMed] [Google Scholar]
  23. Isobe, T., Ichimura, T., Sunaya, T., Okuyama, T., Takahashi, N., Kuwano, R., and Takahashi, Y. (1991). Distinct forms of the protein kinase-dependent activator of tyrosine and tryptophan hydroxylases.J. Mol. Biol.217:125–132. [DOI] [PubMed] [Google Scholar]
  24. Jaeger, C. B., Teitelman, G., Joh, T. H., Albert, V. R., Park, D. H., and Reis, D. J. (1983). Some neurons of the rat central nervous system contain aromatic-L-amino-acid decarboxylase but not monoamines.Science219:1233–1235. [DOI] [PubMed] [Google Scholar]
  25. Kotrschal, K., Krautgartner, W. D., and Adam, H. (1985). Distribution of aminergic neurons in the brain of the sterlet,Acipenser ruthenus (Chondrostei, Actinopterygii).J. Hirnforsch.26:65–72. [PubMed] [Google Scholar]
  26. Lewis, D. A., Melchitzky, D. S., and Haycock J. W. (1993). Four isoforms of tyrosine hydroxylase are expressed in human brain.Neuroscience54:477–492. [DOI] [PubMed] [Google Scholar]
  27. Mouchet, P., Manier, M., Dietl, M., Feuerstein, C., Berod, A., Arluison, M., Denoroy, L., and Thibault, J. (1986). Immunohistochemical study of catecholaminergic cell bodies in the rat spinal cord.Brain Res. Bull.16:341–353. [DOI] [PubMed] [Google Scholar]
  28. Nagatsu, I., Sakai, M., Yoshida, M., and Nagatsu, T. (1988). Aromatic L-amino acid decarboxylase-immunoreactive neurons in and around the cerebrospinal fluid-contacting neurons of the central canal do not contain dopamine or serotonin in the mouse and rat spinal cord.Brain Res.475:91–102. [DOI] [PubMed] [Google Scholar]
  29. Ochi, J., Yamamoto, T., and Hosoya, Y. (1979). Comparative study of the monoamine system in the spinal cord of the lamprey and hagfish.Arch. Histol. Jpn.42:327–336. [DOI] [PubMed] [Google Scholar]
  30. Okado, N., Ishihara, R., Ito, R., Homma, S., and Kohno, K. (1991). Immunohistochemical study of tyrosine-hydroxylase-positive cells and fibers in the chicken spinal cord.Neurosci. Res.11: 108–118. [DOI] [PubMed] [Google Scholar]
  31. Parent, A., and Northcutt, R. G. (1982). The monoamine-containing neurons in the brain of the garfish,Lepisosteus Osseus. Brain Res. Bull.9:189–204. [DOI] [PubMed] [Google Scholar]
  32. Pindzola, R. R., Ho, R. H., and Martin, G. F. (1990). Development of catecholaminergic projections to the spinal cord in the North American opossum,Didelphis virginiana.J. Comp. Neurol.294:399–417. [DOI] [PubMed] [Google Scholar]
  33. Ridet, J.-L., Sandillon, F., Rajaofetra, N., Geffard, M., and Privat, A. (1992). Spinal dopaminergic system of the rat: light and electron, microscopic study using an antiserum against dopamine, with particular emphasis on synaptic incidence.Brain Res.598:233–241. [DOI] [PubMed] [Google Scholar]
  34. Roberts, B. L., and Meredith, G. E. (1987) Immunohistochemical study of a dopaminergic system in the spinal cord of the ray,Raja radiata.Brain Res.437:171–175. [DOI] [PubMed] [Google Scholar]
  35. Roberts, B. L., Meredith, G. E., and Maslam, S. (1989). Immunocytochemical analysis of the dopamine system in the brain and spinal cord of the European eel,Anguilla anguilla.Anat. Embryol.180:401–412. [DOI] [PubMed] [Google Scholar]
  36. Sakai, K., Karasawa, N., Yamada, K., Fujii, T., Takagi, I., and Nagatsu, I. (1992). Immunocytochemical localization of monoaminergic neurons in the brain of grass parakeet (Melopsittacus undulatus).Biogenic Amines9:183–193. [Google Scholar]
  37. Santer, R. M. (1977). Monaminergic nerves in the central and peripheral nervous systems of fishes.Gen. Pharmac.8:157–172. [DOI] [PubMed] [Google Scholar]
  38. Shirouzu, M., Anraku, T., Iwashi, T. A., and Yoshida, M. (1990). A new dopaminergic terminal plexus in the ventral horn of the spinal cord. Immunohistochemical studies at the light and electron microscopic levels.Experientia46:201–204. [DOI] [PubMed] [Google Scholar]
  39. Sims, T. J. (1977). The development of monoamine-containing neurons in the brain and spinal cord of the salamanderAmbystoma mexicanum.J. Comp. Neurol.173:281–318. [DOI] [PubMed] [Google Scholar]
  40. Sims, T. J. (1986). Identification of a second type of catecholaminergic neuron in the spinal cord of the Axolotl salamander.Exp. Neurol.93:428–433. [DOI] [PubMed] [Google Scholar]
  41. Singer, H. S., Coyle, J. T., Vernon, N., Kallman, C. H., and Price, D. L. (1980). The development of catecholaminergic innervation in chick spinal cord.Brain Res.191:417–428. [DOI] [PubMed] [Google Scholar]
  42. Singhaniyom, W., Wreford, N. G. M., and Güldner, F.-H. (1983). Asymmetric distribution of catecholamine-containing neuronal perikarya in the upper cervical spinal cord of the rat.Neurosci. Lett.41:91–97. [DOI] [PubMed] [Google Scholar]
  43. Smeets, W. J. A. J., and Gonzalez, A. (1990). Are putative dopamine-accumulating cell bodies in the hypothalamic periventricular organ a primitive brain character of non-mammalian vertebrates?Neurosci. Lett.114:248–252. [DOI] [PubMed] [Google Scholar]
  44. Smeets, W. J. A. J., and Steinbusch, H. W. M. (1990). New insights into the reptilian catecholaminergic systems as revealed by antibodies against the neurotransmitters and their synthetic enzymes.J. Chem. Neuroanat.3:25–43. [PubMed] [Google Scholar]
  45. Steeves, J. D., Taccogna, C. A., Bell, K. A., and Vincent, S. R. (1987). Distribution of phenylethanolamine-N-methyltransferase (PNMT)-immunoreactive neurons in the avian brain.Neurosci. Lett.76:7–12. [DOI] [PubMed] [Google Scholar]
  46. Stuesse, S. L., Cruce, W. L. R., and Northcutt, R. G. (1990). Distribution of tyrosine hydroxylase-and serotonin-immunoreactive cells in the central nervous system of the thornback guitarfish,Platyrhinoidis triseriata.J. Chem. Neuroanat.3:45–58. [PubMed] [Google Scholar]
  47. Uda, K., Okamura, H., Murakami, S., Nagatsu, I., and Ibata, Y. (1987). Regional distribution of tyrosine hydroxylase immunoreactive neuronal elements in the rat and monkey spinal cord.Biogen. Amines4:153–162. [Google Scholar]
  48. Wallace, J. A., Allgood, P. C., Hoffman, T. J., Mondragon, R. M., and Maez, R. R. (1986). Analysis of the change in number of serotonergic neurons in the chick spinal cord during embryonic development.Brain Res. Bull.17:297–305. [DOI] [PubMed] [Google Scholar]
  49. Wallace, J. A., Hoffman, T. C., Mondragon, R. M., Maez, R. R., and Allgood, P. C. (1987a). Tyrosine hydroxylase (TH)-immunoreactive neurons occur within the spinal cord of the chicken from hatching through adulthood.Soc. Neurosci. Abstr.13:1336. [Google Scholar]
  50. Wallace, J. A., Mondragon, R. M., Allgood, P. C., Hoffman, T. J., and Maez, R. R. (1987b). Two populations of tyrosine hydroxylase-positive cells occur in the spinal cord of the chick embryo and hatchling.Neurosci. Lett.83:253–258. [DOI] [PubMed] [Google Scholar]
  51. Wallace, J. A., Vallejos, A. J., Romero, A. A., Allgood, P. C., and Lopez-Colberg, I. (1989). Development of tyrosine hydroxylase (TH)-immunoreactive neurons in the chick embryonic brain.Soc. Neurosci. Abstr.15:1015. [Google Scholar]
  52. Watson, S. J., and Ellison, J. P. (1976). Cryostat technique for central nervous, system histofluorescence.Histochemistry50:119–127. [DOI] [PubMed] [Google Scholar]
  53. Wolters, J. G., Ten Donkelaar, H. J., and Verhofstad, A. A. J. (1984). Distribution of catecholamines in the brain stem and spinal cord of the lizardVaranus exanthematicus: An immunohistochemical study based on the use of antibodies to tyrosine hydroxylase.Neuroscience13:469–493. [DOI] [PubMed] [Google Scholar]
  54. Wolters, J. G., de Vente, J., and Steinbusch, H. W. M. (1988). An atlas of the dopaminergic system in the rat brain, based on immunohistochemistry using antibodies to dopamine.Eur. J. Neurosci. Suppl.1:287. [Google Scholar]

Articles from Cellular and Molecular Neurobiology are provided here courtesy of Springer

RESOURCES