Advertisement

Acta Biologica Hungarica

, Volume 54, Issue 1, pp 35–44 | Cite as

Cerebrospinal Fluid Contacting Neurons in the Reduced Brain Ventricular System of the Atlantic Hagfish, Myxine glutinosa

  • C. Dávid
  • C. L. Frank
  • Á. Lukáts
  • Á. Szél
  • B. VíghEmail author
Open Access
Article

Abstract

Cerebrospinal fluid (CSF)-contacting neurons are sensory-type cells sending ciliated dendritic process into the CSF. Some of the prosencephalic CSF-contacting neurons of higher vertebrates were postulated to be chemoreceptors detecting the chemical composition of the CSF, other cells may percieve light as “deep encephalic photoreceptors”. In our earlier works, CSF-contacting neurons of the mechanoreceptor-type were described around the central canal of the hagfish spinal cord. It was supposed that perceiving the flow of the CSF they are involved in vasoregulatory mechanisms of the nervous tissue. In the present work, we examined the brain ventricular system of the Atlantic hagfish with special reference to the presence and fine structure of CSF-contacting neurons.

Myxinoids have an ontogenetically reduced brain ventricular system. In the adult hagfish (Myxine glutinosa) the lumen of the lateral ventricle is closed, the third ventricle has a preoptic-, infundibular and subhabenular part that are not connected to each other. The choroid plexus is absent. The infundibular part of the third ventricle has a medial hypophyseal recess and, more caudally, a paired lateral recess. We found CSF-contacting neurons in the lower part of the third ventricle, in the preoptic and infundibular recess as well as in the lateral infundibular recesses.

No CSF-contacting neurons were found in the cerebral aqueduct connecting the subhabenular recess to the fourth ventricle. There is a pineal recess and a well-developed subcommissural organ at the rostral end of the aqueduct. Extending from the caudal part of the fourth ventricle in the medulla to the caudal end of the spinal cord, the central canal has a dorsal and ventral part. Dendrites of CSF-contacting neurons are protruding into the ventral lumen. Corroborating the supposed choroid plexus-like function of the wall of the dorsal central canal, segmental vessels reach a thin area on both sides of the ependymal lining.

The perikarya of the CSF-contacting neurons found in the brain ventricles are mainly bipolar and contain granular vesicles of various size. The bulb-like terminal of their ventricular dendrites bears several stereocilia and contains basal bodies as well as mitochondria. Basal bodies emit cilia of the 9 +0-type. Cilia may arise from the basal body and accessory basal body as well. The axons run ependymofugally and enter - partially cross - the periventricular synaptic zones. No neurohemal terminals similar to those formed by spinal CSF-contacting neurons of higher vertebrates have been found in the hagfish. We suppose that CSF-contacting neurons transform CSF-mediated non-synaptic information taken up by their ventricular dendrites to synaptic one. A light-sensitive role for some (preoptic?) groups of CSF-contacting neurons cannot be excluded.

Keywords

Third ventricle preoptic recess Reissner’s fiber central canal ultrastructure 

Notes

Acknowledgement

This work was supported by grants from the Hungarian Scientific Research Fund (OTKA), Nos T 032860 and T 29048.

References

  1. 1.
    Adam, H. (1956) Der III. Ventrikel und die mikroskopische Struktur seiner Wände bei Lampetra (Petromyzon) fluviatilis L. und Myxine glutinosa nebst einigen Bemerkungen über das Infundibularorgan von Branchiostoma (Amphioxus) lanceolatus Pall. Progr. Neurobiol. (Amst.) 1, 146–158.Google Scholar
  2. 2.
    Adam, H. (1957) Beitrag zur Kenntnis der Hirnventrikel und des Ependyms bei den Cyclostomen. Anat. Anz. 103, 173–188.Google Scholar
  3. 3.
    Bone, Q. (1936) The central nervous system. In: Brodal, A., Fänge R. (eds) The Biology of the Myxine. Skandinavian University Books, Oslo, pp. 50–91.Google Scholar
  4. 4.
    Crosby, E., Schnitzlein, H. N. (1974) The comparative anatomy of the telencephalon of the hagfish, Myxine glutinosa. J. Hirnforsch. 15, 211–236.PubMedGoogle Scholar
  5. 5.
    Donald, J. A., Toop, T., Evans, D. H. (1999) Natriuretic peptide bindind sites in the brain of the Atlantic hagfish, Myxine glutinosa. J. Exp. Zool. 284, 407–413.CrossRefGoogle Scholar
  6. 6.
    Edinger, L. (1906) Über das Gehirn von Myxine glutinosa. Abh. Königl. Preus. Akad. 190, 1–36.Google Scholar
  7. 7.
    Foster, R. G., Grace, M. S., Provencio, I., Degrip, W. J., Garcia-Fernandez, J. M. (1994) Identification of vertebrate deep brain photoreceptors. Neurosci. Behav. Rev. 18, 541–546.CrossRefGoogle Scholar
  8. 8.
    Holm, F. (1901) The finer anatomy of the nervous system of Myxine glutinosa. Morphol. Jahrb. 29, 365–401.Google Scholar
  9. 9.
    Holmgren, N. (1919) Zur Anatomie des Gehirnes von Myxine. Kgl. Svenska Vet.-Akad. Handl. 60, 1–96.Google Scholar
  10. 10.
    Holmgren, N. (1946) On two embryos of Myxine glutinosa. Acta Zool. (Stockh.) 27, 1–90.CrossRefGoogle Scholar
  11. 11.
    Jansen, J. (1930) The brain of Myxine glutinosa. J. Comp. Neurol. 49, 359–507.CrossRefGoogle Scholar
  12. 12.
    Jirikowski, G., Erhardt, G., Grimmelikhuizen, C. J. P., Triepel, J., Patzner, R. A. (1984) FMRFamide-like immunoreactivity in the brain and pituitary of the hagfish, Eptatretus burgeri (Cyclostomata). Cell Tissue Res. 237, 362–366.CrossRefGoogle Scholar
  13. 13.
    Kadota, T. (1991) Distribution of 5HT (serotonnin) immunoreactivity in the central nervous system of the inshore hagfish, Eptatretus burgeri. Cell Tiss. Res. 266, 107–116.CrossRefGoogle Scholar
  14. 14.
    Kadota, T., Goris, R. C., Kusunoki, T. (1993) Dopamine neurons in the hagfish brain. Anat. Record Suppl. 1, 69.Google Scholar
  15. 15.
    Olsson, R. (1959) The neurosecretory hypothalamus system and the adenohypophysis of Myxine. Z. Zellforsch. 51, 97–107.CrossRefGoogle Scholar
  16. 16.
    Ooka-Souda, S., Kadota, T., Kabasawa, H. (1993) The preoptic nucleus: the probable location of the circadian pacemaker of the hagfish, Eptatretus burgeri. Neurosci. Lett. 164, 33–36.CrossRefGoogle Scholar
  17. 17.
    Ooka-Souda, S., Kadota, T., Kabasawa, H., Takeuchi, H. (1995) A possible retinal information route to the circadian pacemaker through pretectal areas in the hagfish, Eptatretus burgeri. Neurosci. Lett. 192, 201–204.CrossRefGoogle Scholar
  18. 18.
    Retzius, G. (1893) Das Gehirn und das Auge von Myxine. Biol. Untersuch. N. F. 5, 55–68.Google Scholar
  19. 19.
    Tsuneki, K. (1986) A survey of occurrence of about seventeen circumventricular organs in brains of various vertebrates with special reference to lower groups. J. Hirnforsch. 27, 441–470.Google Scholar
  20. 20.
    Ueck, M., Kobayashi, H. (1979) Neue Ergebnisse zu Fragen der vergleichenden Epiphysen-forschung. Verh. Anat. Ges. 73, 961–963.Google Scholar
  21. 21.
    Vígh, B., Vígh-Teichmann, I. (1971) Structure of the medullo-spinal liquor contacting neuronal system. Acta Biol. Hung. 22, 227–243.Google Scholar
  22. 22.
    Vígh, B., Vígh-Teichmann, I. (1982) The cerebrospinal fluid-contacting neurosecretory cell: A pro-toneuron. In: Farner, D. S., Lederis, K. (eds) Molecules, Cells Systems. Plenum Press, New York, pp. 458–460.Google Scholar
  23. 23.
    Vígh, B., Vígh-Teichmann, I. (1991) The double central canal of Myxine glutinosa: presence of CSF-contacting neurons and glial labyrinth. Anat. Anz. (Suppl.) 172, 332.Google Scholar
  24. 24.
    Vígh, B., Vígh-Teichmann, I. (1992) Cytochemistry of CSF-contacting neurons and pinealocytes. Progr. Brain Res. 91, 299–306.CrossRefGoogle Scholar
  25. 25.
    Vígh, B., Vígh-Teichman, I. (1998) Actual problems of the cerebrospinal fluid contacting neurons. Microsc. Res. Techn. 41, 57–83.CrossRefGoogle Scholar
  26. 26.
    Vígh, B., Vígh-Teichmann, I., Aros, B. (1969) Das Paraventricularorgan und das Liquorkontakt-Neuronensystem. Anat. Anz. 125, 683–688.Google Scholar
  27. 27.
    Vígh, B., Vígh-Teichmann, I., Koritsánszky, S., Aros, B. (1970) Ultrastruktur der Liquorkontakt-neurone des Rückenmarkes von Reptilien. Z. Zellforsch. 109, 180–194.CrossRefGoogle Scholar
  28. 28.
    Vígh, B., Vígh-Teichmann, I., Aros, B. (1971) Ultrastruktur der spinalen Liquorkontaktneurone beim Krallenfrosch (Xenopus laevis). Z. Zellforsch. 112, 201–211.CrossRefGoogle Scholar
  29. 29.
    Vígh, B., Manzano, M. J., Zádori, A., Frank, C. L., Lukáts, Á., Röhlich, P., Szél, Á., Dávid, C. (2002) Nonvisual photoreceptors of the deep brain, pineal organs and retina. Histol. Histopathol (in press).Google Scholar
  30. 30.
    Vígh-Teichmann, I., Vígh, B. (1974) The infundibular cerebrospinal fluid-contacting neurons. Ergebn. Anat. Entwickl. Gesch. 50, 1–91.Google Scholar
  31. 31.
    Vígh-Teichmann, I., Vígh, B. (1983) The system of cerebrospinal fluid contacting neurons. Arch. Histol. Japon. 46, 427–468.CrossRefGoogle Scholar
  32. 32.
    Vígh-Teichmann, I., Vígh, B. (1989) The cerebrospinal fluid-contacting neuron: a peculiar cell type of the central nervous system. Immunocytochemical aspects. Arch. Histol.Cytol. 52, 195–207.CrossRefGoogle Scholar
  33. 33.
    Vígh-Teichmann, I., Vígh, B., Olsson R., Van Veen, Th. (1984) Opsin immunoreactive outer segments of photoreceptors in the eye and in the lumen of the optic nerve of the hagfish, Myxine glutinosa. Cell Tissue Res. 238, 515–522.CrossRefGoogle Scholar
  34. 34.
    Wächtler, K. (1975) The distribution of acetylcholinesterase in the cyclostome brain. II. Myxine glutinosa. Cell Tiss. Res. 159, 109–120.Google Scholar
  35. 35.
    Wernadakis, A. J., Bemis, W. E., Bittman, E. L. (1998) Localization and partial characterization of melatonin receptors in amphyoxus, hagfish, lamprey, and skate. Gen. Comp. Endocrinol. 110, 67–78.CrossRefGoogle Scholar
  36. 36.
    Wicht, U., Northcutt, R. G. (1992) FMRFamide-like immunoreactivity in the brain of the Pacific hag-fish, Eptatretus stouti. Cell Tissue Res. 270, 443–449.CrossRefGoogle Scholar
  37. 37.
    Wicht, U., Northcutt, R. G. (1994) An immunohistochemical study of the telencephalon and dien-cephalon in a myxinoid jawless fish, the Pacific hagfish, Eptatretus stouti. Brain Behav. Evol. 43, 140–161.CrossRefGoogle Scholar
  38. 38.
    Worthington, J. (1905) Contribution to our knowledge of the myxinoids. Am. Naturalist 39, 625–668.CrossRefGoogle Scholar

Copyright information

© Akadémiai Kiadó, Budapest 2003

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

  • C. Dávid
    • 1
  • C. L. Frank
    • 1
  • Á. Lukáts
    • 1
  • Á. Szél
    • 1
  • B. Vígh
    • 1
    Email author
  1. 1.Department of Human Morphology and Developmental BiologySemmelweis UniversityBudapestHungary

Personalised recommendations