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Serotonergic Intraventricular Axons in the habenular region

Phagocytosis after induced degeneration

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Summary

Both intracerebroventricular injection of 5,7-dihydroxytryptamine and electrolytical midbrain-raphe lesions in rats induce degeneration of supraependymal axons (SEAs) normally occurring in large numbers upon the ependyma of the medial habenular nucleus and habenular commissure. It is concluded that the intraventricular axon plexus in the epithalamic region is comprised of serotonergic (5-HT) fibers originating in the dorsal and/or median raphe nuclei. Besides the elimination of SEAs, conspicious features were a marked reduction in the number of cilia, degenerative signs in the habenular ependyma, and the emergence of large numbers of supraependymal macrophages, being most probably involved in phagocytosis of the axonal debris. It is suggested that the nucleus habenulae medialis is influenced serotonergically by the midbrain raphe via (1) a direct projection upon its neurons and (2) an indirect projection by way of the intraventricular axon plexus. The origin of intraventricular macrophages is discussed in relation to recent data in the literature.

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References

  • Aghajanian, G.K., Gallager, D.W.: Raphe origin of serotonergic nerves terminating in the cerebral ventricles. Brain Res. 88, 221–231 (1975)

    Google Scholar 

  • Aghajanian, G.K., Wang, R.Y.: Habenular and other midbrain raphe afferents demonstrated by a modified retrograde tracing technique. Brain Res. 122, 229–242 (1977)

    Google Scholar 

  • Akagi, K., Powell, E.W.: Differential projections of habenular nuclei. J. Comp. Neurol. 132, 263–274 (1968)

    Google Scholar 

  • Ariëns Kappers, J.: Beitrag zur experimentellen Untersuchung von Funktion und Herkunft der Kolmerschen Zellen des Plexus chorioideus beim Axolotl und Meerschweinchen. Z. Anat. Entw. Gesch. 117, 1–19 (1953)

    Google Scholar 

  • Björklund, A., Nobin, A., Stenevi, U.: The use of neurotoxic dihydroxytryptamines as tools for morphological studies and localized lesioning of central indoleamine neurons. Z. Zellforsch. 145, 479–501 (1973)

    Google Scholar 

  • Bleier, R.: Surface fine structure of supraependymal elements and ependyma of hypothalamic third ventricle of mouse. J. Comp. Neurol. 161, 555–568 (1975)

    Google Scholar 

  • Bleier, R.: Ultrastructure of supraependymal cells and ependyma of hypothalamic third ventricle of mouse. J. Comp. Neurol. 174, 359–376 (1977)

    Google Scholar 

  • Bleier, R., Albrecht, R., Cruce, J.A.F.: Supraependymal cells of hypothalamic third ventricle. Identification as resident phagocytes of the brain. Science 189, 299–301 (1975)

    Google Scholar 

  • Bleier, R., Marsh, R.: Reaction of third ventricular ependyma and supraependymal cells to vascular stomatitis virus. In: Scanning Electron Microscopy (SEM Inc., AMF O'Hare, Il. 60666, U.S.A.), II, 1978, pp. 29–36

    Google Scholar 

  • Bobillier, P., Seguin, S., Petitjean, F., Salvert, D., Touret, M., Jouvet, M.: The raphe nuclei of the cat brain stem: a topographical atlas of their efferent projections as revealed by autoradiography. Brain Res. 113, 449–486 (1976)

    Google Scholar 

  • Breese, G.R., Cooper, B.R.: Behavioral and biochemical interactions of 5,7-dihydroxytryptamine with various drugs when administered intracisternally to adult and developing rats. Brain Res. 98, 517–527 (1975)

    Google Scholar 

  • Calas, A., Bosler, O., Arluison, M., Bouchaud, C.: Serotonin as a neurohormone in circumventricular organs and supraependymal fibers. In: Brain-Endocrine interaction. III. Neural hormones and reproduction. pp. 238–250 Basel: Karger 1978

    Google Scholar 

  • Carpenter, S.J., McCarthy, L.E., Borison, H.L.: Electron microscopic study on the epiplexus (Kolmer) cells of the cat choroid plexus. Z. Zellforsch. 110, 471–486 (1970)

    Google Scholar 

  • Chan-Palay, V.: Serotonin axons in the supra-and subependymal plexuses and in the leptomeninges; their roles in local alterations of cerebrospinal fluid and vasomotor activity. Brain Res. 102, 103–130 (1976)

    Google Scholar 

  • Chan-Palay, V.: Cerebellar dentate nucleus; organization, cytology and transmitters. pp. 390–454 Berlin: Springer, 1977

    Google Scholar 

  • Coates, P.W.: Supraependymal cells in recesses of the monkey third ventricle (1). Am. J. Anat. 136, 533–539 (1973)

    Google Scholar 

  • Coates, P.W.: Supraependymal cells and fiber processes in the fetal monkey third ventricle: correlated scanning and transmission electron microscopy. In: Scanning Electron Microscopy (SEM Inc., AMF O'Hare, Il. 60666, U.S.A.), II, pp. 143–150 (1978)

    Google Scholar 

  • Conrad, L.C.A., Leonard, C.M., Pfaff, D.W.: Connections of the median and dorsal raphe nuclei in the rat: an autoradiographic and degeneration study. J. Comp. Neurol. 156, 179–206 (1974)

    Google Scholar 

  • Cupédo, R.N.J.: The surface ultrastructure of the habenular complex of the rat. Anat. Embryol. 152, 43–64 (1977)

    Google Scholar 

  • Dahlström, A., Fuxe, K.: Evidence for the existence of monoamine-containing neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brain stem neurons. Acta Physiol. Scand. 62 (suppl. 232), 3–56 (1964)

    Google Scholar 

  • De Groot, J.: The rat forebrain in stereotaxic coordinates, second ed., Amsterdam: N.V. Noord-Hollandsche Uitgevers Mij., 1963

    Google Scholar 

  • Descarries, L., Beaudet, A., Watkins, K.C.: Serotonin nerve terminals in adult rat neocortex. Brain Res. 100, 563–588 (1975)

    Google Scholar 

  • Gottesfeld, Z., Hoover, D.B., Muth, E.A., Jacobowitz, D.M.: Lack of biochemical evidence for a direct habenulo-raphe GABAergic pathway. Brain Res. 141, 353–356 (1978)

    Google Scholar 

  • Herkenham, M., Nauta, W.J.H.: Afferent connections of the habenular nuclei in the rat. A horseradish peroxidase study, with a note on the fiber-of-passage problem. J. Comp. Neurol. 173, 123–146 (1977)

    Google Scholar 

  • Hetzel, W.: Ependymal structures of the anterior and inferior horn of the lateral ventricles of the rabbit brain. In: Scanning Electron Microscopy (SEM Inc., AMF O'Hare, I1. 60666, U.S.A.), II, pp. 129–136 (1978)

    Google Scholar 

  • König, J.F.R., Klippel, R.A.: The rat brain. A stereotaxic atlas of the forebrain and lower parts of the brain stem. Baltimore: Williams and Wilkins Comp. 1963

    Google Scholar 

  • Kolmer, W.: Über eine eigenartige Beziehung von Wanderzellen zu den Chorioidealplex des Gehirns der Wirbeltiere. Anat. Anz. 54, 15–19 (1921)

    Google Scholar 

  • Leslie, R.A., Gwyn, D.G., Morrison, C.M.: The fine structure of the ventricular surface of the area postrema of the cat with particular reference to supraependymal structures. Am. J. Anat. 153, 273–290 (1978)

    Google Scholar 

  • Lorez, H.P., Richards, J.G.: Distribution of indolealkylamine nerve terminals in the ventricles of the rat brain. Z. Zellforsch. 144, 511–522 (1973)

    Google Scholar 

  • Lorez, H.P., Richards, J.G.: Effects of intracerebroventricular injection of 5,6-dihydroxytryptamine and 6-hydroxydomamine on supraependymal nerves. Brain Res. 116, 165–171 (1976)

    Google Scholar 

  • Lorez, H.P., Pieri, L., Richards, J.G.: Disappearance of supraependymal 5-HT axons in the rat forebrain after electrolytic and 5,6-DHT-induced lesions of the medial forebrain bundle. Brain Res. 100, 1–12 (1975)

    Google Scholar 

  • Mestres, P.: Development of supraependymal structures in the rat hypothalamus. In: Scanning Electron Microscopy (SEM Inc., AMF O'Hare, I1. 60666, U.S.A.), II, pp. 549–554, 1978

    Google Scholar 

  • Mestres, P., Breipohl, W.: Morphology and distribution of supraependymal cells in the third ventricle of the albino rat. Cell Tissue Res. 168, 303–314 (1976)

    Google Scholar 

  • Moore, R.Y., Halaris, A.E., Jones, B.E.: Serotonin neurons of the midbrain raphe: ascending projections. J. Comp. Neurol. 180, 417–438 (1978)

    Google Scholar 

  • Nauta, W.J.H.: Hippocampal projections and related neural pathways to the midbrain in the cat. Brain 81, 319–340 (1958)

    Google Scholar 

  • Palkovits, M., Saavedra, J.M., Jacobowitz, D.M., Kizer, J.S., Záborsky, L., Brownstein, M.J.: Serotonergic innervation of the forebrain: effect of lesions on serotonin and tryptophan hydroxylase levels. Brain Res. 130, 121–134 (1977)

    Google Scholar 

  • Pasquier, D.A., Anderson, C., Forbes, W.B., Morgane, P.J.: Horseradish peroxidase tracing of the lateral habenular-midbrain raphe nuclei connections in the rat. Brain Res. Bull. 1, 443–451 (1976)

    Google Scholar 

  • Ribas, J.L.: The rat epithalamus. I., Correlative scanning-transmission electron microscopy of supraependymal nerves. Cell Tissue Res. 182, 1–16 (1977)

    Google Scholar 

  • Richards, J.G.: Autoradiographic evidence for the selective accumulation of [3H]5-HT by supraependymal nerve terminals. Brain Res. 134, 151–157 (1977)

    Google Scholar 

  • Richards, J.G., Tranzer, J.P.: Ultrastructural evidence for the localization of an indolealkylamine in supra-ependymal nerves from combined cytochemistry and pharmacology. Experientia (Basel) 30, 287–289 (1974)

    Google Scholar 

  • Richards, J.G., Lorez, H.P., Tranzer, J.P.: Indolealkylamine nerve terminals in cerebral ventricles: identification by electron microscopy and fluorescence histochemistry. Brain Res. 57, 277–288 (1973)

    Google Scholar 

  • Sakai, K., Salvert, D., Touret, M., Jouvet, M.: Afferent connections of the nucleus raphe dorsalis in the cat visualized by the horseradish peroxidase technique. Brain Res. 137, 11–35 (1977)

    Google Scholar 

  • Scott, D.E., Krobisch-Dudley, G., Paull, W.K., Kozlowski, G.P., Ribas, J.: The primate median eminence. I. Correlative scanning-transmission electron microscopy. Cell Tissue Res. 162, 61–73 (1975)

    Google Scholar 

  • Scott, D.E., Krobisch-Dudley, G., Paull, W.K., Kozlowski, G.P.: The ventricular system in neuroendocrine mechanisms. III. Supraependymal neuronal networks in the primate brain. Cell Tissue Res. 179, 235–254 (1977)

    Google Scholar 

  • Taber-Pierce, E., Foote, W.E., Hobson, J.A.: The efferent connections of the nucleus raphe dorsalis. Brain Res. 107, 137–144 (1976)

    Google Scholar 

  • Walsh, R.J., Brawer, J.R., Sun Lin, P.: Supraependymal cells in the third ventricle of the neonatal rat. Anat. Rec. 190, 257–270 (1978)

    Google Scholar 

  • Wang, R.Y., Aghajanian, G.K.: Antidromically identified serotonergic neurons in the rat midbrain raphe. Brain Res. 132, 186–193 (1977a)

    Google Scholar 

  • Wang, R.Y., Aghajanian, G.K.: Physiological evidence for habenula as major link between forebrain and midbrain raphe. Science 197, 89–91 (1977b)

    Google Scholar 

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Cupédo, R.N.J., de Weerd, H. Serotonergic Intraventricular Axons in the habenular region. Anat Embryol 158, 213–226 (1980). https://doi.org/10.1007/BF00315907

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