Skip to main content
Log in

The distribution of monoamine oxidase and acetylcholinesterase in the brain of Xenopus laevis tadpoles

  • Published:
Zeitschrift für Zellforschung und Mikroskopische Anatomie Aims and scope Submit manuscript

Summary

The distribution of monoamine oxidase (MAO) in the brain of Xenopus laevis tadpoles (stage 52–56) was studied histochemically with a modified Glenner's tryptamine-tetrazolium method. A moderate activity was observed in fibre regions of the striatum and septum (including the medial and lateral forebrain bundles), in the neuropil of the nucleus amygdalae, in the commissura anterior and commissura hippocampi, in the fibre regions of the diencephalon (including the optic chiasma), in the fibre regions of the tectum opticum and the tegmentum of the mesencephalon and in the white substance of the ventral half of the medulla oblongata. A greater MAO activity was found in the neuropil of the entire nucleus praeopticus. In the partes anterior and magnocellularis of this nucleus, MAO positive fibres are present in close contact with the perikarya, indicating a monoaminergic innervation of these neurons. The perikarya themselves did not show MAO activity. In the neurons of the nucleus praeopticus epichiasmaticus, the paraventricular organ (PVO) and nucleus infundibularis dorsalis (NID), only a slight MAO activity has been demonstrated in the perikarya, whereas a strong MAO positivity was found in the intraventricular protrusions and the neuropil. These data indicate the aminergic character of the neurons of these nuclei. From the postoptic fibre region a MAO positive tract was observed towards the developing median eminence and pars intermedia of the hypophysis. The pars nervosa and some cells of the pars distalis also contained MAO. Along the border of the aquaeduct of Silvius and the fourth ventricle, MAO positive liquor-containing neurons are also present.

The distribution of acetylcholinesterase (AChE) was investigated in the hypothalamohypophysial region. AChE activity was found in the neuropil of the nucleus praeopticus magnocellularis, in the fibres of the optic chiasma and in the postoptic fibre region. The neurons of the PVO and NID were AChE negative. An AChE positive tract could be traced from the postoptic fibre region to the developing median eminence and pars nervosa. The pars distalis did not show AChE activity. However, in tadpoles reaching the metamorphic climax, ChE activity appeared in certain cells of the pars distalis; this might be related to degenerative phenomena in the acidophilic cells. The absence of AChE activity in the pars intermedia indicates a regulation of MSH release by peptidergic nerves to be unlikely.

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

  • Bartels, W.: Die Ontogenese der aminhaltigen Neuronensysteme im Gehirn von Rana temporaria. Z. Zellforsch. 116, 94–118 (1971).

    Google Scholar 

  • Baumgarten, H. G., Björklund, A., Holstein, A. F., Nobin, A.: Organization and ultrastructural identification of the catecholamine nerve terminals in the neural lobe and pars intermedia of the rat pituitary. Z. Zellforsch. 126, 483–517 (1972).

    Google Scholar 

  • Björklund, A.: Monoamine-containing fibres in the neuro-intermediate lobe of the pig and rat. Z. Zellforsch. 89, 573–589 (1968).

    Google Scholar 

  • Björklund, A., Falck, B.: Histochemical characterization of a tryptamine-like substance stored cells of the mammalian adenohypophysis. Acta physiol. scand. 77, 475–489 (1969).

    Google Scholar 

  • Braak, H.: Biogene Amine im Gehirn vom Frosch (Rana esculenta). Z. Zellforsch. 106, 269–308 (1970).

    Google Scholar 

  • Cohen, A. G.: Observations of the pars intermedia of Xenopus laevis. Nature (Lond.) 215, 55–56 (1967).

    Google Scholar 

  • Cottle, M. K. W., Silver, A.: Histochemical demonstration of acetylcholinesterase in the hypothalamus of the female guinea pig. Z. Zellforsch. 103, 570–588 (1970).

    Google Scholar 

  • Doerr-Schott, J., Follenius, E.: Localisation des fibres aminergiques dans l'hypophyse de Rana esculenta. Etude autoradiographique au microscope électronique. C. R. Acad. Sci. (Paris) 269, 737–740 (1969).

    Google Scholar 

  • Doerr-Schott, J., Follenius, E.: Innervation de l'hypophyse intermédiaire de Rana esculenta, et identification des fibres aminergiques par autoradiographie au microscope électronique. Z. Zellforsch. 106, 99–118 (1970).

    Google Scholar 

  • Enemar, A., Falck, B.: On the presence of adrenergic nerves in the pars intermedia of the frog, Rana temporaria. Gen. comp. Endocr. 5, 577–583 (1965).

    Google Scholar 

  • Enemar, A., Falck, B., Iturriza, F. C.: Adrenergic nerves in the pars intermedia of the pituitary in the toad, Bufo arenarum. Z. Zellforsch. 77, 325–330 (1967).

    Google Scholar 

  • Follett, B. K., Kobayashi, H., Farner, D. S.: The distribution of monoamine oxidase and acetylcholinesterase in the hypothalamus and its relation to the hypothalamo-hypophysial neurosecretory system in the white-crowned sparrow, Zonotrichia leucophrys gambellii. Z. Zellforsch. 75, 57–65 (1966).

    Google Scholar 

  • Glenner, G. G., Burtner, H. J., Brown, G. R.: The histochemical demonstration of monoamine oxidase activity by tetrazolium salts. J. Histochem. Cytochem. 5, 591–600 (1957).

    Google Scholar 

  • Goos, H. J. Th.: Hypothalamic control of the pars intermedia in Xenopus laevis tadpoles. Z. Zellforsch. 97, 118–124 (1969).

    Google Scholar 

  • Goos, H. J. Th., Halewijn, R. van: Biogenic amines in the hypothalamus of Xenopus laevis tadpoles. Naturwissenschaften 55, 393–394 (1968).

    Google Scholar 

  • Haase, E., Farner, D. S.: Acetylcholinesterase in der Pars distalis von Zonotrichia leucophrys gambelii (Aves). Z. Zellforsch. 93, 356–368 (1969).

    Google Scholar 

  • Haase, E., Farner, D. S.: Investigations of the butyrylcholinesterase-containing cells of the adenohypophysis of the white-crowned sparrow, Zonotrichia leucophrys gambelii. Z. Zellforsch. 118, 570–578 (1971).

    Google Scholar 

  • Herrick, C. J.: The amphibian forebrain. VI. Necturus. J. comp. Neurol. 58, 1–289 (1933).

    Google Scholar 

  • Hopkins, C. R.: Localization of adrenergic fibers in the amphibian pars intermedia by electron microscope autoradiography and their selective removal by 6-hydroxydopamine. Gen. comp. Endocr. 16, 112–120 (1971).

    Google Scholar 

  • Iijima, K., Shantha, T. R., Bourne, G. H.: Enzyme-histochemical studies on the hypothalamus with special reference to the supraoptic and paraventricular nuclei of the squirrel monkey (Saimiri sciureus). Z. Zellforsch. 79, 76–91 (1967).

    Google Scholar 

  • Imai, K.: Color change and pituitary function in Xenopus laevis. In: Biology of normal and abnormal melanocytes (eds. T. Kawamura, T. B. Fitzpatrick and M. Seiji), p. 17–30. Baltimore-London-Tokyo: University Park, Press 1971.

    Google Scholar 

  • Ito, T.: Changes in skin color and fine structure of the intermediate pituitary gland of the frog, Rana nigromaculata, after extirpation of the median eminence. Neuroendocrinology 8, 180–197 (1971).

    Google Scholar 

  • Iturriza, F. C.: Electronmicroscopic study of the pars intermedia of the pituitary of the toad, Bufo arenarum. Gen. comp. Endocr. 4, 492–502 (1964).

    Google Scholar 

  • Jansen, W. F., West, R.: A cytochemical investigation of specific and non-specific cholinesterase activity in the saccus vasculosus of the rainbow trout. Proc. kon. ned. Akad. Wet., Series C 74, 344–351 (1971).

    Google Scholar 

  • Kabawata, I.: Electron microscopy of the rat hypothalamic neurosecretory system. I. The supraoptic nuclei of normal and dehydrated rats. Gunma Symp. Endocr. 1, 51–58 (1964).

    Google Scholar 

  • Karnovsky, M. J., Roots, L.: A “direct-coloring” thiocholine method for cholinesterases. J. Histochem. Cytochem. 12, 219–220 (1964).

    Google Scholar 

  • Kerr, T.: The development of the pituitary in Xenopus laevis Daudin. Gen. comp. Endocr. 6, 303–311 (1966).

    Google Scholar 

  • Kobayashi, H., Urano, A., Yokoyama, K.: Acetylcholinesterase (AChE) and monoamine oxidase (MAO) in the hypothalamic neurosecretory system. Proc. 3rd Intern. Congr. Histochem. Cytochem. p. 129–130 (1968).

  • Konstantinova, M.: The effect of adrenaline and acetylcholine on the hypothalamo-hypophysial neurosecretion in the rat. Z. Zellforsch. 83, 549–567 (1967).

    Google Scholar 

  • Matsui, T., Kobayashi, H.: Histochemical demonstration of monoamine oxidase in the hypothalamo-hypophysial system of the tree sparrow and the rat. Z. Zellforsch. 68, 172–182 (1965).

    Google Scholar 

  • Murakami, M.: Elektronenmikroskopische Untersuchung der neurosekretorischen Zellen im Hypothalamus der Maus. Z. Zellforsch. 56, 277–299 (1962).

    Google Scholar 

  • Nakai, Y.: Electron microscopic observations on synapse-like contacts between pituicytes and different types of nerve fibers in the anuran pars nervosa. Z. Zellforsch. 110, 27–39 (1970).

    Google Scholar 

  • Nakai, Y., Gorbman, A.: Evidence for a double innervated secretory unit in the anuran pars intermedia. II. Electron microscopic studies. Gen. comp. Endocr. 13, 108–116 (1969).

    Google Scholar 

  • Nieuwkoop, P. D., Faber, J.: Normal table of Xenopus laevis Daudin. Amsterdam: North-Holland Publishing Co. 1956.

    Google Scholar 

  • Novikoff, A. B., Shin, W. Y., Drucker, J.: Cold acetone fixation for enzyme localization in frozen sections. J. Histochem. Cytochem. 8, 37–40 (1960).

    Google Scholar 

  • Olsson, K.: Effects on water diuresis of infusions of transmitter substances into the 3rd ventricle. Acta physiol. scand. 79, 133–135 (1970).

    Google Scholar 

  • Oordt, P. G. W. J. van, Goos, H. J. Th., Peute, J., Terlou, M.: Hypothalamo-hypophysial relations in amphibian larvae. Gen. comp. Endocr., Suppl. 3, 41–50 (1972).

  • Pehlemann, F. W.: Ultrastructure and innervation of the pars intermedia of the pituitary of Xenopus laevis. Gen. comp. Endocr. 9, 481 (1967).

    Google Scholar 

  • Peterson, R. P.: Synapses in the rat supraoptic nucleus. Anat. Rec. 151, 399 (1965).

    Google Scholar 

  • Peute, J.: Fine structure of the paraventricular organ of Xenopus laevis tadpoles. Z. Zellforsch. 97, 564–575 (1969).

    Google Scholar 

  • Peute, J.: Ultrastructural aspects of the nucleus infundibularis dorsalis in the hypothalamus of Xenopus laevis. Z. Zellforsch. 137, 513–520 (1973).

    Google Scholar 

  • Peute, J., Goos, H. J. Th.: Biogenic amines in the tuber cinereum of Xenopus laevis. Electron and fluorescence microscopical observations. Aspects of neuroendocrinology (eds. W. Bargmann, B. Scharrer) p. 111–117. Berlin-Heidelberg-New York: Springer 1970.

    Google Scholar 

  • Polenov, A L., Senchik, J. I.: Synapses on neurosecretory cells of the supraoptic nucleus in white mice. Nature (Lond.) 211, 1423–1424 (1966).

    Google Scholar 

  • Saland, L. C.: Ultrastructure of the frog pars intermedia in the relation to hypothalamic control of hormone release. Neuroendocrinology 3, 72–88 (1968).

    Google Scholar 

  • Terlou, M., Ploemacher, R. E.: The distribution of monomamine in the tel-, di- and mesencephalon of Xenopus laevis tadpoles, with special reference to the hypothalamo-hypophysial system. Z. Zellforsch. 137, 521–540 (1973).

    Google Scholar 

  • Uemura, H.: Cholinesterases in the hypothalamo-hypophysial system of the bird, Zosterops palpebrosa japonica. Zool. Mag. (Japan) 73, 118–126 (1964).

    Google Scholar 

  • Uemura, H.: Histochemical studies on the distribution of cholinesterase and alkaline phosphatase in the vertebrate neurosecretory system. Annot. Zool. Jap. 38, 79–96 (1965).

    Google Scholar 

  • Urano, A.: Monoamine oxidase in the hypothalamic neurosecretory system and the adenohypophysis of the Japanese quail and the mouse. J. Fac. Univ. Tokyo Section IV, 11, 437–451 (1968).

    Google Scholar 

  • Urano, A.: Monoamine oxidase in the hypothalamo-hypophysial region of the brown smooth dogfish, Triakis scyllia. Endocr. jap. 18, 37–46 (1971a).

    Google Scholar 

  • Urano, A.: Monoamine oxidase in the hypothalamo-hypophysial region of the teleosts, Anguilla japonica and Oryzias latipes. Z. Zellforsch. 114, 83–94 (1971b).

    Google Scholar 

  • Urano, A.: Monoamine oxidase in the neurohypophysis of the newt (Cynops pyrrhogaster pyrrhogaster), the toad (Bufo bufo japonicus) and the tortoise (Clemmys japonica). Z. Zellforsch. 126, 454–465 (1972).

    Google Scholar 

  • Vigh, B.: The paraventricular organ, its structure and function. In: Zirkumventrikuläre Organe und Liquor. Symposium Reinhardsbrunn (Hrsg. G. Sterba), S. 148–150. Jena: Fischer 1969.

    Google Scholar 

  • Vigh, B.: Das Paraventrikularorgan und das Zirkumventrikuläre System. Studia Biologica Hungarica, Bd. 10, Budapest: Akadémiai Kiadó 1971.

    Google Scholar 

  • Vigh-Teichmann, I., Vigh, B., Aros, B.: Enzymhistochemische Studien am Nervensystem. IV. Acetylcholinesteraseaktivität im Liquorkontakt — Neuronensystem verschiedener Vertebraten. Histochemie 21, 322–337 (1970).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

The stimulating interest and helpful advice of Prof. Dr. P. G. W. J. van Oordt is gratefully acknowledged. Thanks are also due to Mr. H. van Kooten and his co-workers for making the photographs.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Terlou, M., Stroband, H.W.J. The distribution of monoamine oxidase and acetylcholinesterase in the brain of Xenopus laevis tadpoles. Z.Zellforsch 140, 261–275 (1973). https://doi.org/10.1007/BF00306698

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00306698

Key words

Navigation