Advertisement

Acta Biologica Hungarica

, Volume 60, Issue 4, pp 333–346 | Cite as

Distribution of Oxytocin-Immunoreactive Neuronal Elements in the Rat Spinal Cord

  • Julianna JójártEmail author
  • I. Jójárt
  • Krisztina Boda
  • Márta Gálfi
  • A. Mihály
  • Zs. B. Baldauf
  • M. Vecsernyés
Article

Abstract

We investigated the distribution of oxytocin in rat spinal cord using immunocytochemistry and radioimmunoassay (RIA). Each segment of the spinal cord from cervical to coccygeal contained oxytocin-immunoreactive fibers. The Rexed laminae I and II of the dorsal horn showed moderate to intense immunoreactivity. A dense network was found around the central canal where some fibers apposed the ependyma. The autonomic centers of the spinal cord at the thoracolumbar and sacral segments were heavily innervated. Few fibers were found around the motoneurons. In the white matter, the immunoreactivity was localized mainly in the dorsal part of the lateral funiculus, in the pars funicularis of the nucleus intermediolateralis and in a longitudinal network of the lateral funiculus below the spinal cord surface. Some fibers from this network entered the pia mater. RIA measurements revealed that the cervical spinal cord had lower oxytocin content than that found in either the thoracic, lumbar, sacral or coccygeal region. Our results show that the distribution of oxytocin-immunoreactive fibers in the spinal cord correlates with anatomic locations related to nociceptive, autonomic and motor functions. We assume that oxytocin-containing axons play a role in secreting oxytocin directly into the liquor space of the spinal cord.

Keywords

Oxytocin distribution immunocytochemistry radioimmunoassay spinal cord 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

We thank Prof. Tj. B. Van Wimersma Greidanus for providing the antibody to oxytocin. We are grateful to Prof. B. Penke and Prof. L. Siklós for their constant support and valuable suggestions. The excellent technical assistance of Gabriella Papp, J. Szeles, M. Dezső and Z. Imre is greatly acknowledged.

References

  1. 1.
    Argiolas, A., Melis, M. R. (2004) The role of oxytocin and the paraventricular nucleus in the sexual behaviour of male mammals. Physiol. Behav. 83, 309–317.PubMedGoogle Scholar
  2. 2.
    Arletti, R., Benelli, A., Bertolini, A. (1993) Influence of oxytocin on nociception and morphine antinociception. Neuropeptides 24, 125–129.PubMedGoogle Scholar
  3. 3.
    Benoussaidh, A., Maurin, Y., Rampin, O. (2004) Spinal effects of oxytocin on uterine motility in anesthetized rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287, R446–R453.PubMedGoogle Scholar
  4. 4.
    Buijs, R. M. (1978) Intra- and extrahypothalamic vasopressin and oxytocin pathways in the rat. Pathways to the limbic system, medulla oblongata and spinal cord. Cell Tiss. Res. 192, 423–435.Google Scholar
  5. 5.
    Buijs, R. M. (1980) Vasopressin and Oxytocin Innervation of the Rat Brain. A Light- and Electron-microscopical Study. PhD Thesis, Amsterdam.Google Scholar
  6. 6.
    Buijs, R. M. (1983) Vasopressin and oxytocin–their role in neurotransmission. Pharmac. Ther. 22, 127–141.Google Scholar
  7. 7.
    Condés-Lara, M., González, N. M., Martínez-Lorenzana, G., Delgado, O. L., Freund-Mercier, M. J. (2003) Actions of oxytocin and interactions with glutamate on spontaneous and evoked dorsal spinal cord neuronal activities. Brain Res. 976, 75–81.PubMedGoogle Scholar
  8. 8.
    Daddona, M. M., Haldar, J. (1994) Opioid modulation of oxytocin release from spinal cord synapto-somes. Neuroreport 5, 1833–1835.PubMedGoogle Scholar
  9. 9.
    Dogterom, J., Van Wimersma Greidanus, T. B., Swaab, D. F. (1977) Evidence for the release of vaso-pressin and oxytocin into cerebrospinal fluid: measurements in plasma and CSF of intact and hypophysectomized rats. Neuroendocrinology 24, 108–118.PubMedGoogle Scholar
  10. 10.
    Gibson, S. J., Polak, J. M., Bloom, S. R., Wall, P. D. (1981) The distribution of nine peptides in rat spinal cord with special emphasis on the substantia gelatinosa and on the area around the central canal (lamina X). J. Comp. Neurol. 201, 65–79.PubMedGoogle Scholar
  11. 11.
    Gilbey, M. P., Coote, J. H., Fleetwood-Walker, S., Peterson, D. F. (1982) The influence of the par-aventriculo-spinal pathway, and oxytocin and vasopressin on sympathetic preganglionic neurones. Brain Res. 251, 283–290.PubMedGoogle Scholar
  12. 12.
    Hallbeck, M., Larhammar, D., Blomqvist, A. (2001) Neuropeptide expression in rat paraventricular hypothalamic neurons that project to the spinal cord. J. Comp. Neurol. 433, 222–238.PubMedGoogle Scholar
  13. 13.
    Hawthorn, J., Ang, V. T. Y., Jenkins, J. S. (1985) Effect of lesions in the hypothalamic paraventricular, supraoptic and suprachiasmatic nuclei on vasopressin and oxytocin in rat brain and spinal cord. Brain Res. 346, 51–57.PubMedGoogle Scholar
  14. 14.
    Hosoya, Y., Matsukawa, M., Okado, N., Sugiura, Y., Kohno, K. (1995) Oxytocinergic innervation to the upper thoracic sympathetic preganglionic neurons in the rat. A light and electron microscopical study using a combined retrograde transport and immunocytochemical technique. Exp. Brain Res. 107, 9–16.PubMedGoogle Scholar
  15. 15.
    Jenkins, J. S., Ang, V. T., Hawthorn, J., Rossor, M. N., Iversen, L. L. (1984) Vasopressin, oxytocin and neurophysins in the human brain and spinal cord. Brain Res. 291, 111–117.PubMedGoogle Scholar
  16. 16.
    Jójárt, I., Vecsernyés, M., Jójárt, J., Laczi, F., Szabó, G., Kovács, G. L., Janáky, T., László, F. A., Telegdy, G. (1989) Acute effects of peripheral histamine administration on arginine-8-vasopressin and oxytocin levels in rat spinal cord. Endocrinologia Experimentalis 23, 229–233.PubMedGoogle Scholar
  17. 17.
    Krukoff, T. L., Ciriello, J., Calaresu, F. R. (1985) Segmental distribution of peptide- and 5HT-like immunoreactivity in nerve terminals and fibers of the thoracolumbar sympathetic nuclei of the cat. J. Comp. Neurol. 240, 103–116.PubMedGoogle Scholar
  18. 18.
    Lang, R. E., Heil, J., Ganten, D., Hermann, K., Rascher, W., Unger, T. (1983) Effect of lesions in the paraventricular nucleus of the hypothalamus on vasopressin and oxytocin contents in brainstem and spinal cord of rat. Brain Res. 260, 326–329.PubMedGoogle Scholar
  19. 19.
    Loup, F., Tribollet, E., Dubois-Dauphin, M., Pizzolato, G., Dreifuss, J. J. (1989) Localization of oxytocin biding sites in the human brainstem and upper spinal cord: an autoradiographic study. Brain Res. 500, 223–230.PubMedGoogle Scholar
  20. 20.
    Lowry, O. H., Rosebrough, N. J., Farr, A. L., Randall, R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265–275.Google Scholar
  21. 21.
    Lukic, D., Haldar, J. (1993) Isotonic and hypertonic saline act as stressful stimuli for oxytocinergic system of the pituitary, hypothalamus and spinal cord. Life Sci. 53, 579–584.PubMedGoogle Scholar
  22. 22.
    Miaskowski, C., Ong, G. L., Haldar, J. (1987) Cyclic variations in spinal cord levels of oxytocin and vasopressin during the stages of the rat estrous cycle. Endocrinology 120, 1685–1687.PubMedGoogle Scholar
  23. 23.
    Miaskowski, C., Ong, G. L., Lukic, D., Haldar, J. (1988) Immobilization stress affects oxytocin and vasopressin levels in hypothalamic and extrahypothalamic sites. Brain Res. 458, 137–141.PubMedGoogle Scholar
  24. 24.
    Nilaver, G., Zimmerman, E. A., Wilkins, J., Michaels, J., Hoffman, D., Silverman, A. J. (1980) Magnocellular hypothalamic projections to the lower brain stem and spinal cord of the rat. Immuno-cytochemical evidence for predominance of the oxytocin-neurophysin system compared to the vaso-pressin-neurophysin system. Neuroendocrinol. 30, 150–158.Google Scholar
  25. 25.
    Pandita, R. K., Nylén, A., Andersson, K.-E. (1998) Oxytocin-induced stimulation and inhibition of bladder activity in normal conscious rats–influence of nitric oxide synthase inhibition. Neuroscience 85, 1113–1119.Google Scholar
  26. 26.
    Petras, J. M., Cummings, J. F. (1972) Autonomic neurons in the spinal cord of the rhesus monkey: a correlation of the findings of cytoarchitectonics and sympathectomy with fiber degeneration following dorsal rhizotomy. J. Comp. Neurol. 146, 189–218.PubMedGoogle Scholar
  27. 27.
    Pittman, Q. J., Riphagen, C. L., Lederis, K. (1984) Release of immunoassayable neurohypophyseal peptides from rat spinal cord, in vivo. Brain Res. 300, 321–326.PubMedGoogle Scholar
  28. 28.
    Raggenbass, M. (2001) Vasopressin- and oxytocin-induced activity in the central nervous system: electrophysiological studies using in-vitro systems. Prog. Neurobiol. 64, 307–326.PubMedGoogle Scholar
  29. 29.
    Reiter, M. K., Kremarik, P., Freund-Mercier, M. J., Stoeckel, M. E., Desaulles, E., Feltz, P. (1994) Localization of oxytocin binding sites in the thoracic and upper lumbar spinal cord of the adult and postnatal rat: a histoautoradiographic study. Eur. J. Neurosci. 6, 98–104.PubMedGoogle Scholar
  30. 30.
    Robinson, D. A., Wei, F., Wang, G. D., Li, P., Kim, S. J., Vogt, S. K., Muglia, L. J., Zhuo, M. (2002) Oxytocin mediates stress-induced analgesia in adult mice. J. Physiol. 540, 593–606.PubMedPubMedCentralGoogle Scholar
  31. 31.
    Rousselot, P., Papadopoulos, G., Merighi, A., Poulain, D. A., Theodosis, D. T. (1990) Oxytocinergic innervation of the rat spinal cord. An electron microscopic study. Brain Res. 529, 178–184.PubMedGoogle Scholar
  32. 32.
    Sansone, G. R., Gerdes, C. A., Steinman, J. L., Winslow, J. T., Ottenweller, J. E., Komisaruk, B. R., Insel, T. R. (2002) Vaginocervical stimulation releases oxytocin within the spinal cord in rats. Neuroendocrinology 75, 306–315.PubMedGoogle Scholar
  33. 33.
    Sansone, G. R., Komisaruk, B. R. (2001) Evidence that oxytocin is an endogenous stimulator of autonomic sympathetic preganglionics: the pupillary dilatation response to vaginocervical stimulation in the rat. Brain Res. 898, 265–271.PubMedGoogle Scholar
  34. 34.
    Sawchenko, P. E., Swanson, L. W. (1982) Immunohistochemical identification of neurons in the paraventricular nucleus of the hypothalamus that project to the medulla or to the spinal cord in the rat. J. Comp. Neurol. 205, 260–272.PubMedGoogle Scholar
  35. 35.
    Silverman, A.-J., Zimmerman, E. A. (1983) Magnocellular neurosecretory system. Ann. Rev. Neurosci. 6, 357–380.PubMedGoogle Scholar
  36. 36.
    Sofroniew, M. V. (1980) Projections from vasopressin, oxytocin, and neurophysin neurons to neural targets in the rat and human. J. Histochem. Cytochem. 28, 475–478.PubMedGoogle Scholar
  37. 37.
    Sofroniew, M. V. (1985) Vasopressin, oxytocin and their related neurophysins. In: Björklund, A., Hökfelt, T. (eds) Handbook of Chemical Neuroanatomy. Vol. 4: GABA and Neuropeptides in the CNS, Part I, Elsevier, Amsterdam, pp. 93–165.Google Scholar
  38. 38.
    Sofroniew, M. V., Weindl, A. (1978) Extrahypothalamic neurophysin-containing perikarya, fiber pathways and fiber clusters in the rat brain. Endocrinology 102, 334–337.Google Scholar
  39. 39.
    Sofroniew, M. V., Weindl, A., Schrell U., Wetzstein, R. (1981) Immunohistochemistry of vaso-pressin, oxytocin and neurophysin in the hypothalamus and extrahypothalamic regions of the human and primate brain. Acta Histochem. Suppl. 24, 79–95.PubMedGoogle Scholar
  40. 40.
    Sternberger, L. A., Hardy, P. H., Jr., Cuculis, J. J., Meyer, H. G. (1970) The unlabeled antibody enzyme method of immunohistochemistry. Preparation and properties of soluble antigen-antibody complex (horseradish peroxidase-antihorseradish peroxidase) and its use in identification of spirochetes. J. Histochem. Cytochem. 18, 315–333.PubMedGoogle Scholar
  41. 41.
    Swanson, L. W., McKellar, S. (1979) The distribution of oxytocin- and neurophysin-stained fibers in the spinal cord of the rat and monkey. J. Comp. Neurol. 188, 87–106.PubMedGoogle Scholar
  42. 42.
    Tribollet, E., Barberis, C., Arsenijevic, Y. (1997) Distribution of vasopressin and oxytocin receptors in the rat spinal cord: sex-related differences and effect of castration in pudendal motor nuclei. Neuroscience 78, 499–509.PubMedGoogle Scholar
  43. 43.
    White, J. D., Krause, J. E., McKelvy, J. F. (1986) In vivo biosynthesis and transport of oxytocin, vasopressin and neurophysin from the hypothalamus to the spinal cord. Neuroscience 17, 133–140.Google Scholar
  44. 44.
    Yang, J., Yang, Y., Chen J.-M., Liu, W.-Y., Wang, C.-H., Lin, B.-C. (2007) Central oxytocin enhances antinociception in the rat. Peptides 28, 1113–1119.PubMedGoogle Scholar
  45. 45.
    Yang, Z., Wheatley, M., Coote, J. H. (2002) Neuropeptides, amines and amino acids as mediators of the sympathetic effects of paraventricular nucleus activation in the rat. Exp. Physiol. 87, 663–674.Google Scholar
  46. 46.
    Yu, S.-Q., Lundeberg, T., Yu, L.-C. (2003) Involvement of oxytocin in spinal antinociception in rats with inflammation. Brain Res. 983, 13–22.PubMedGoogle Scholar

Copyright information

© Akadémiai Kiadó, Budapest 2009

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  • Julianna Jójárt
    • 1
    Email author
  • I. Jójárt
    • 2
  • Krisztina Boda
    • 3
  • Márta Gálfi
    • 4
  • A. Mihály
    • 1
  • Zs. B. Baldauf
    • 1
  • M. Vecsernyés
    • 5
  1. 1.Department of AnatomyUniversity of SzegedSzegedHungary
  2. 2.Department of MedicineErzsébet HospitalHódmezővásárhelyHungary
  3. 3.Department of Medical InformaticsUniversity of SzegedSzegedHungary
  4. 4.University of Szeged, Gyula Juhász Faculty of EducationInstitute of Applied Natural ScienceSzegedHungary
  5. 5.Pharmaceutical Technology DepartmentUniversity of DebrecenDebrecenHungary

Personalised recommendations