Skip to main content
Log in

Immunohistochemical examination of intraspinal serotonin neurons and fibers in the chicken lumbar spinal cord and coexistence with Leu-enkephalin

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Intraspinal serotonin-positive cells and fibers were examined in the chicken lumbar spinal cord following removal of descending serotonin fibers by spinal transection. Co-localization of Leu-enkephalin immunoreactivity in intraspinal serotonin cells was also examined using a double immunofluorescence labeling technique. By one or two weeks after spinal transection, virtually all supraspinal serotonin fibers were eliminated. Intraspinal serotonin cells were located ventral or ventrolateral to the central canal corresponding to laminae VII, VIII, and IX, and the anterior funiculus. Intraspinal serotonin cells sent fibers to (1) the pia mater on the ventral or ventrolateral surface of the spinal cord; (2) vessels in the spinal cord; (3) sympathetic preganglionic column of Terni; (4) other intraspinal serotonin neurons; (5) the central canal. Some 30%–50% of the intraspinal serotonin cells co-localized with Leu-enkephalin. Intraspinal serotonin fibers co-containing Leu-enkephalin were observed in the pia mater located on the most lateral surface of the spinal cord.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adams JC (1981) Heavy metal intensification of DAB-based HRP reaction product. J Histochem Cytochem 29:775

    Google Scholar 

  • Bowker RM (1986) Intrinsic 5HT-immunoreactive neurons in the spinal cord of the fetal non-human primate. Dev Brain Res 28:137–143

    Google Scholar 

  • Bowker RM, Westlund KN, Coulter JD (1981) Origins of serotonergic projections to the spinal cord in rat: an immunocytochemical-retrograde transport study. Brain Res 226:187–199

    Google Scholar 

  • Cabot JB, Wild JM, Choen DH (1979) Raphe inhibition of sympathetic preganglionic neurons. Science 203:184–186

    Google Scholar 

  • Cabot JB, Reiner A, Bogan N (1982) Avian bulbospinal pathways: anterograde and retrograde studies of cells of origin, funicular trajectories and laminar terminations. Prog Brain Res 57: 79–108

    Google Scholar 

  • Chan-Palay V, Jonsson G, Palay SL (1978) Serotonin and substance P coexist in neurons of the rat's central nervous system. Proc Natl Acad Sci USA 75:1582–1586

    Google Scholar 

  • Edvinsson L, MacKenzie ET (1977) Amine mechanisms in the cerebral circulation. Pharmacol Rev 28:275–348

    Google Scholar 

  • Gilbey MP, Coote JH, Macleod VH, Peterson DF (1981) Inhibition of sympathetic activity by stimulating in the raphe nuclei and the role of 5-hydroxytryptamine in this effect. Brain Res 226:131–142

    Google Scholar 

  • Griffith SG, Lincoln J, Burnstock G (1982) Serotonin as a neurotransmitter in cerebral arteries. Brain Res 247:388–392

    Google Scholar 

  • Harris-Warrick RM, McPhee JC, Filler JA (1985) Distribution of serotonergic neurons and processes in the lamprey spinal cord. Neuroscience 14:1141–1147

    Google Scholar 

  • Hökfelt T, Ljungdahl A, Steinbusch H, Verhofstad A, Nilsson G, Brodin E, Pernow B, Goldstein M (1978) Immunohistochemical evidence of substance P-like immunoreactivity in some 5-hydroxytryptamine-containing neurons in the rat central nervous system. Neuroscience 3:517–538

    Google Scholar 

  • Hosoya Y, Yaginuma H, Okado N, Kohno K (1992) Morphology of sympathetic preganglionic neurons innervating the superior cervical ganglion in the chicken: an immunohistochemical study using retrograde labeling of cholera toxin subunit B. Exp Brain Res 89:478–483

    Google Scholar 

  • Johansson O, Hökfelt T, Pernow B, Jeffcoate SL, White N, Steinbusch HWM, Verhofstad AAJ, Emson PC, Spindel E (1982) Immunohistochemical support for three putative transmitters in one neuron: coexistence of 5-hydroxytryptamine, substance P- and thyrotropin-releasing hormone-like immunoreactivity in medullary neurons projecting to the spinal cord. Neuroscience 6:1857–1881

    Google Scholar 

  • Johnson DG, De Nogueria C, Araujo GM (1981) A simple method of reducing the fading of immunofluorescence during microscopy. J Immunol Methods 43:349–350

    Google Scholar 

  • Kojima M, Takeuchi Y, Goto M, Sano Y (1982) Immunohistochemical study on the distribution of serotonin fibers in the spinal cord of the dog. Cell Tissue Res 226:477–491

    Google Scholar 

  • Kojima M, Takeuchi Y, Goto M, Sano Y (1983) Immunohistochemical study on the localization of serotonin fibers and terminals in the spinal cord of the monkey (Macaca fuscata). Cell Tissue Res 229:23–26

    Google Scholar 

  • LaMotte CC, Johns DR, Lanerolle NC de (1982) Immunohistochemical evidence of indolamine neurons in monkey spinal cord. J Comp Neurol 206:359–370

    Google Scholar 

  • Macdonald RL, Cohen DH (1970) Cells of origin of sympathetic pre- and postganglionic cardioacceleratory fibers in the pigeon. J Comp Neurol 140:343–358

    Google Scholar 

  • Martin AH (1979) A cytoarchitechtonic scheme of the spinal cord of the domestic fowl, Gallus gallus domesticus: lumbar region. Acta Morphol Neerl-Scand 17:105–117

    Google Scholar 

  • Millhorn DE, Hökfelt T, Verhofstad AAJ, Terenius L (1989) Individual cells in the raphe nuclei of the medulla oblongata in rat that contain immunoreactivities for both serotonin and enkephalin project to the spinal cord. Exp Brain Res 75:536–542

    Google Scholar 

  • Newton BW, Hamill RW (1988) The morphology and distribution of rat serotoninergic intraspinal neurons: an immunohistochemical study. Brain Res Bull 20:349–360

    Google Scholar 

  • Newton BW, Maley B, Hamill RW (1986) Immunohistochemical demonstration of serotonin neurons in autonomic regions of the rat spinal cord. Brain Res 376:155–163

    Google Scholar 

  • Newton BW, Burkhart AH, Hamill RW (1989) Immunohistochemical distribution of serotonin in spinal autonomic nuclei. II. Early and late postnatal ontogeny in the rat. J Comp Neurol 279:82–103

    Google Scholar 

  • Ochi J, Hosoya Y (1974) Fluorescence microscopic differentiation of monoamines in the hypothalamus and spinal cord of the lamprey, using a new filter system. Histochemistry 40: 263–266

    Google Scholar 

  • Okado N, Ishihara R, Ito R, Homma S, Kohno K (1991a) Immunohistochemical study of tyrosine-hydroxylase-positive cells and fibers in the chicken spinal cord. Neurosci Res 11:108–118

    Google Scholar 

  • Okado N, Matsukawa M, Noritake S, Ozaki S, Hamada S, Arita M, Kudo N (1991b) Species differences in the distribution and coexistence ratio of serotonin and substance P in the monkey, cat, rat and chick spinal cord. Neurosci Lett 132:155–158

    Google Scholar 

  • Okado N, Sako H, Homma S, Ishikawa K (1992) Development of serotoninergic system in the brain and spinal cord of the chick. Prog Neurobiol 38:93–123

    Google Scholar 

  • Ozaki S, Kudo N, Okado N (1992) Immunohistochemical study on development of serotonin-, substance P- and enkephalin-positive fibers in the rat spinal motor nucleus. J Comp Neurol 325:462–470

    Google Scholar 

  • Parent A, Northcutt RG (1982) The monoamine-containing neurons in the brain of the garfish, Lepisosteus osseus. Brain Res Bull 9:189–204

    Google Scholar 

  • Rajaofetra N, Passagia J-G, Marlier L, Poulat P, Pellas F, Sandillon F, Verschuere B, Gouy D, Geffard M, Privat A (1992) Serotoninergic, noradrenergic, and peptidergic innervation of Onuf's nucleus of normal and transected spinal cords of baboons (Papio papio). J Comp Neurol 318:1–17

    Google Scholar 

  • Reddy VK, Cassini P, Ho RH, Martin GF (1990) Origins and terminations of bulbospinal axons that contain serotonin and either enkephalin or substance-P in the North American opossum. J Comp Neurol 294:96–108

    Google Scholar 

  • Ritchie TC, Roos LJ, Williams BJ, Leonard RB (1984) The descending and intrinsic serotoninergic innervation of an elasmobranch spinal cord. J Comp Neurol 224:395–406

    Google Scholar 

  • Sako H, Kojima T, Okado N (1986a) Immunohistochemical study on the development of serotoninergic neurons in the chick: II. distribution of cell bodies and fibers in the spinal cord. J Comp Neurol 253:79–91

    Google Scholar 

  • Sako H, Kojima T, Okado N (1986b) Immunohistochemical study on the development of serotoninergic neurons in the chick: I. Distribution of cell bodies and fibers in the brain. J Comp Neurol 253:61–78

    Google Scholar 

  • Sano Y, Takeuchi Y, Yamada H, Ueda S, Goto S (1982) Immunohistochemical studies on the serotoninergic innervation of the pia mater. Histochemistry 76:277–280

    Google Scholar 

  • Tashiro T, Satoda T, Takahashi O, Matsushima R, Mizuno R (1988) Distribution of axons exhibiting both enkephalin- and serotonin-like immunoreactivities in the lumbar cord segments: an immunohistochemical study in the cat. Brain Res 440:357–362

    Google Scholar 

  • Tashiro T, Satoda T, Matsushima R, Mizuno N (1990) Distribution of axons showing both enkephalin- and serotonin-like immunoreactivities in the lumbar cord segments of the Japanese monkey (Macaca fuscata). Brain Res 512:143–146

    Google Scholar 

  • Van Dongen PAM, Hökfelt T, Grillner S, Rehfeld JF, Verhofstad AJ (1985a) A cholecystokinin-like peptide is present in 5-hydroxytryptamine neurons in the spinal cord of the lamprey. Acta Physiol Scand 125:557–560

    Google Scholar 

  • Van Dongen PAM, Hökfelt T, Grillner S, Verhofstad AAJ, Steinbusch HWM, Cuello AC, Terenius L (1985b) Immunohistochemical demonstration of some putative neurotransmitters in the lamprey spinal cord and spinal ganglia: 5-hydroxytryptamine-, tachykinin-, and neuropeptide-Y-immunoreactive neurons and fibers. J Comp Neurol 234:501–522

    Google Scholar 

  • Wallace JA, Allgood PC, Hoffman TJ, Mondragon RM, Maez RR (1986) Analysis of the change in number of serotonergic neurons in the chick spinal cord during embryonic development. Brain Res Bull 17:297–305

    Google Scholar 

  • Wessendorf MW, Elde R (1987) The coexistence of serotonin- and substance P-like immunoreactivity in the spinal cord of the rat as shown by immunofluorescent double labeling. J Neurosci 7:2353–2363

    Google Scholar 

  • Yamada T, Placzek M, Tanaka H, Dodd J, Jessell TM (1991) Control of cell pattern in the developing nervous system: polarizing activity of the floor plate and notochord. Cell 64:635–647

    Google Scholar 

  • Zamboni L, DeMartino C (1967) Buffered picric acid-formaldehyde: a new rapid fixation for electron microscopy. J Cell Biol 35:148A

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Permanent address: This study was supported by Grant-in-Aid for Scientific Research on Priority Area from the Ministry of Education, Science and Culture, Japan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hamada, S., Ogawa, M. & Okado, N. Immunohistochemical examination of intraspinal serotonin neurons and fibers in the chicken lumbar spinal cord and coexistence with Leu-enkephalin. Cell Tissue Res 282, 387–397 (1995). https://doi.org/10.1007/BF00318871

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00318871

Key words

Navigation