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Studies on central projections of the pineal nerve tract in rainbow trout, Salmo gairdneri Richardson, using cobalt chloride iontophoresis

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Summary

The central projections and terminations of the pineal nerve tract in rainbow trout, Salmo gairdneri, were studied using the cobalt chloride method developed for selectively staining nerve fibres by Pitman et al. (1972). A modification of the method is described for the first time making its use possible in the study of central pathways of the pineal nerve tract.

The pineal tract consists of only pinealofugal fibers which project centrally over an extensive sensorimotor area in the brain. Along its course through the subcommissural-posterior commissure region it gives off several branches:

  1. 1.

    Rostral parapinealward fibers which enter the parenchyma of the parapineal organ with or without terminating here.

  2. 2.

    Prominent habenulaward lateral branches with contralateral and ipsilateral terminations in the lateral habenular nucleus. The contralateral fibers decussate in the habenular commissure.

  3. 3.

    Large number of lateral and lateroventral fibers of small caliber with terminations in the area praetectalis and together with some decussating contralateral fibers in the di- and mesencephalic periventricular grey and partly in the nuclei dorsomedialis and dorsolateralis thalami.

  4. 4.

    Prominent lateral bundles consisting of mainly large caliber fibers and entering the Haubenwulst with terminals on cells in the nucleus of Darkschewitsch and possibly other cells of origin of the medial longitudinal fasciculus. These bundles also give rise to terminals and probably collaterals in the dorsal tegmentum.

The optic tectum and nucleus interpeduncularis are shown to be free of pineal terminals. Convincing evidence is presented showing total absence of pineal terminals in the subcommissural organ in trout. The possibility of direct innervation of the preoptic nucleus by pineal fibers is pointed out.

The results are discussed in the light of existing evidence on pineal tract pathways in fishes as well as from an evolutionary viewpoint. The findings confirm some of the observations of other workers particularly those of Nils Holmgren (1917, 1918 a, b). It is proposed that the lack of success in fully describing the pineal tract pathways in fishes and the prevailing ambivalence are owing to methodological weaknesses and that the pattern of central projections described here for trout may prove to be generally true for other fishes as well. The advantages of cobalt chloride iontophoresis as a method for studying pineal innervation are pointed out.

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References

  • Breder, C. M., Rasquin, P.: Comparative studies on the light sensitivity of blind characins from a series of Mexican caves. Bull. Amer. Mus. Nat. Hist. 89, 325–351 (1947)

    Google Scholar 

  • Breder, C. M., Rasquin, P.: A preliminary report on the role of pineal organ in the control of pigment cells and light reactions in teleosts fishes. Science 111, 10–12 (1950)

    Google Scholar 

  • Brookover, Ch.: The olfactory nerve, the nervous terminalis and the preoptic sympathetic system in Amia calva. J. comp. Neurol. 20, 49–118 (1910)

    Google Scholar 

  • Byrne, J.: Locomotor activity responses in juvenile sockeye salmon, Oncorhynchus nerka to melatonin and serotonin. Canad. J. Zool. 48, 1425–1427 (1970)

    Google Scholar 

  • Dendy, A.: On the parietal sense-organs and associated structures in the New Zealand lamprey (Geotria australis). Quart. J. micr. Sci. 51, 1–29 (1907)

    Google Scholar 

  • Dodt, E.: Photosensitivity of the pineal organ in the teleost Salmo irideus (Gibbons). Experientia (Basel) 19, 642 (1963)

    Google Scholar 

  • Ebbeson, S. O. E.: Quantitative studies of superior cervical sympathetic ganglion in a variety of primates including man. J. Morph. 124, 117–132 (1968)

    Google Scholar 

  • Fenwick, J. C.: The pineal organ: photoperiod and reproductive cycle in the goldfish, Carassius auratus. J. Endocr. 46, 101–111 (1970a)

    Google Scholar 

  • Fenwick, J. C.: Demonstration and effect of melatonin in fish. Gen. comp. Endocr. 14, 86–97 (1970b)

    Google Scholar 

  • Fink, R. P., Heimer, L.: Two methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system. Brain Res. 4, 369–374 (1967)

    Google Scholar 

  • Frisch, K. von: Beiträge zur Physiologie der Pigmentzellen in der Fischhaut. Pflügers Arch. ges. Physiol. 138, 319–387 (1911a)

    Google Scholar 

  • Frisch, K. von: Das Parietalorgan der Fische als funktionierendes Organ. S.-B. Ges. Morph. Physiol. (München) 27, 16–18 (1911b)

    Google Scholar 

  • Hafeez, M. A.: Effect of melatonin on body coloration and spontaneous swimming activity in rainbow trout, Salmo gairdneri. Comp. Biochem. Physiol. 36, 639–656 (1970)

    Google Scholar 

  • Hafeez, M. A.: Light microscopic studies on the pineal organ in teleost fishes with special regard to its function. J. Morph. 134, 281–313 (1971)

    Google Scholar 

  • Hafeez, M. A., Ford, P.: Histology and histochemistry of the pineal organ in the sockeye salmon, Oncorhynchus nerka Walbaum. Canad. J. Zool. 45, 117–126 (1967)

    Google Scholar 

  • Hafeez, M. A., Quay, W. B.: Histochemical and experimental studies of 5-hydroxytryptamine in pineal organs of teleosts (Salmo gairdneri and Atherinopsis californiensis). Gen. comp. Endocr. 13, 211–217 (1969)

    Google Scholar 

  • Hafeez, M. A., Quay, W. B.: The role of the pineal organ in the control of phototaxis and body coloration in rainbow trout (Salmo gairdneri Richardson). Z. vergl. Physiol. 68, 403–415 (1970a)

    Google Scholar 

  • Hafeez, M. A., Quay, W. B.: Pineal acetylserotonin methyltransferase activity in the teleost fishes, Hesperoleucus symmetricus and Salmo gairdneri, with evidence for lack of effect of constant light and darkness. Comp. gen. Pharmacol. 1, 257–262 (1970b)

    Google Scholar 

  • Hanyu, I., Niwa, H.: Pineal photosensitivity in three teleosts, Salmo irideus, Plecoglossus altivelus and Mugil cephalus. Rev. Canad. Biol. 29, 133–140 (1970)

    Google Scholar 

  • Hanyu, I., Niwa, H., Tamura, T.: A slow potential from the epiphysis cerebri of fishes. Vision Res. 9, 621–623 (1969)

    Google Scholar 

  • Haue, F. M. S.: Heavy metals in the brain. Berlin-Heidelberg-New York: Springer 1973

    Google Scholar 

  • Hill, Ch.: The epiphysis of teleosts and Amia. J. Morph. 9, 237–268 (1894)

    Google Scholar 

  • Hoar, W. S.: Phototactic and pigmentary responses of sockeye salmon smolts following injury to the pineal organ. J. Fish. Res. Board Can. 12, 178–185 (1955)

    Google Scholar 

  • Holmgren, N.: Zur Frage der Epiphysen-Innervation bei Teleostiern. Folia neuro-biol. (Lpz.) 10, 1–15 (1917)

    Google Scholar 

  • Holmgren, N.: Über die Epiphysennerven von Clupea sprattus und harengus. Ark. Zool. 11, 25, 1–5 (1918a)

    Google Scholar 

  • Holmgren, N.: Zum Bau der Epiphyse von Squalus acanthias. Ark. Zool. 11, 1–28 (1918b)

    Google Scholar 

  • Holmgren, U.: On the structure of the pineal area of teleost fishes. Göteborgs Kgl. Vetenskaps-Vitterhets-Samhall. Handl. Ser. B 8, 3, 5–66 (1959)

    Google Scholar 

  • Kappers, J. Ariëns: Survey of the innervation of the epiphysis cerebri and the accessory pineal organs of vertebrates. In: Structure and function of the epiphysis cerebri. Progr. in brain research, vol. 10 (J. Ariëns Kappers and J. P. Schadé, eds.), p. 87–153. Amsterdam: Elsevier Publ. 1965

    Google Scholar 

  • Kappers, J. Ariëns: The sensory innervation of the pineal organ in the lizard, Lacerta viridis, with remarks on its position in the trend of pineal phylogenetic structural and functional evolution. Z. Zellforsch. 81, 581–618 (1967)

    Google Scholar 

  • Kappers, C. Ariëns, Huber, G. C., Crosby, E. C.: The comparative anatomy of the nervous system of vertebrates, including man, vol. II. New York: Hafner 1960

    Google Scholar 

  • Kater, S. B., Nicholson, C.: Intracellular staining in neurobiology. Berlin-Heidelberg-New York: Springer 1973

    Google Scholar 

  • Kelley, D. E., van de Kamer, J. C.: Cytological and histochemical investigations on the pineal organ of the adult frog (Rana esculenta). Z. Zellforsch. 52, 618–639 (1960)

    Google Scholar 

  • Llinas, R.: Procion yellow and cobalt as tools for the study of structure-function relationships in vertebrate central nervous systems. In: Intracellular staining in neurobiology (S. B. Kater and C. Nicholson, eds.), p. 211–225. Berlin-Heidelberg-New York: Springer 1973

    Google Scholar 

  • Morita, Y.: Entladungsmuster pinealer Neurone der Regenbogenforelle (Salmo irideus) bei Belichtung des Zwischenhirns. Pflügers Arch. ges. Physiol. 289, 155–167 (1966)

    Google Scholar 

  • Morita, Y., Bergmann, G.: Physiologische Untersuchungen und weitere Bemerkungen zur Struktur des lichtempfindlichen Pinealorgans von Pterophyllum scalare Cuv. et Val. (Cichlidae, Teleostei). Z. Zellforsch. 119, 289–294 (1971)

    Google Scholar 

  • Motte, I. de la: Untersuchungen zur vergleichenden Physiologie der Lichtempfindlichkeit geblendeter Fische. Naturwissenschaften 50, 363 (1963)

    Google Scholar 

  • Motte, I. de la: Untersuchungen zur vergleichenden Physiologie der Lichtempfindlichkeit geblendeter Fische. Z. vergl. Physiol. 49, 58–90 (1964)

    Google Scholar 

  • Mulloney, B.: Microelectrode injection, axonal iontophoresis, and the structure of neurons. In: Intracellular staining in neurobiology (S. B. Kater and C. Nicholson, eds.), p. 99–113. Berlin-Heidelberg-New York: Springer 1973

    Google Scholar 

  • Murakami, M., Tanizaki, T.: An electron microscopic study of the toad subcommissural organ. Arch. histol. Jap. 23, 337–358 (1963)

    Google Scholar 

  • Oksche, A.: Untersuchungen über die Nervenzellen und Nervenverbindungen des Stirnorgans, der Epiphyse und des Subkommissuralorgans bei anuren Amphibien. Morph. Jb. 95, 393–425 (1955)

    Google Scholar 

  • Oksche, A.: The subcommissural organ. Symposium of the International Society for neurovegetative research on neurohormones and neurohumors. Amsterdam, 1967. J. NeuroViscer. Relat., Suppl. IX, 111–139 (1969)

  • Oksche, A.: Sensory and glandular elements of the pineal organ. In: The pineal gland. Symposium of the Ciba Foundation (London, 1970). London: J. &. A. Churchill 1971

    Google Scholar 

  • Oksche, A., Kirschstein, H.: Weitere elektronenmikroskopische Untersuchungen am Pinealorgan von Phoxinus laevis (Teleostei, Cyprinidae). Z. Zellforsch. 112, 572–588 (1971)

    Google Scholar 

  • Oksche, A., Vaupel-von Harnack, M.: Elektronenmikroskopische Untersuchungen an den Nervenbahnen des Pinealkomplexes von Rana esculenta L. Z. Zellforsch. 68, 389–426 (1965)

    Google Scholar 

  • Olsson, R.: Studies on the subcommissural organ. Acta zool. 39, 71–102 (1958)

    Google Scholar 

  • Omura, Y., Oguri, N.: Histological studies on the pineal organ of 15 species of teleosts. Bull. Jap. Soc. scient. Fish. 35, 991–1000 (1969)

    Google Scholar 

  • Owman, Ch., Rüdeberg, C.: Light, fluorescence, and electron microscopic studies on the pineal organ of the pike, Esox lucius L., with special regard to 5-hydroxytryptamine. Z. Zellforsch. 107, 522–550 (1970)

    Google Scholar 

  • Paul, E., Hartwig, H.-G., Oksche, A.: Neurone und zentralnervöse Verbindungen des Pineal-organs der Anuren. Z. Zellforsch. 112, 466–493 (1971)

    Google Scholar 

  • Pihl, E., Falkmer, S.: Trials to modify the sulphide-silver method for ultrastructural tissue localization of heavy metals. Acta histochem. (Jena) 27, 34–41 (1967)

    Google Scholar 

  • Pitman, R. M., Tweedle, C. D., Cohen, M. J.: Branching of central neurons; intracellular cobalt injection for light and electron microscopy. Science 179, 182–184 (1972)

    Google Scholar 

  • Prior, D. J., Fuller, P. M.: The use of cobalt iontophoresis technique for identification of the mesencephalic trigeminal nucleus. Brain Res. 64, 71–74 (1973)

    Google Scholar 

  • Quay, W. B.: Retinal and pineal hydroxyindole-O-methyl transferase activity in vertebrates. Life Sci. 4, 983–991 (1965)

    Google Scholar 

  • Reed, B. L.: The control of circadian pigment changes in the pencil fish: a proposed role for melatonin. Life Sci. 7, 961–974 (1968)

    Google Scholar 

  • Reed, R. L., Finnin, B. C., Ruffin, N. E.: The effect of melatonin and epinephrine on the melanophores of freshwater teleosts. Life Sci. 8, 113–120 (1969)

    Google Scholar 

  • Rüdeberg, C.: Light and electron microscopic studies on the pineal organ of the dogfish Scyliorhinus canicula L. Z. Zellforsch. 96, 548–581 (1969a)

    Google Scholar 

  • Rüdeberg, C.: Structure of the parapineal organ of the adult rainbow trout, Salmo gairdneri Richardson. Z. Zellforsch. 93, 282–304 (1969b)

    Google Scholar 

  • Rüdeberg, C.: Structure of the pineal organs of Anguilla L. and Lebistes reticulatus Peters (Teleostei). Z. Zellforsch. 122, 227–243 (1971)

    Google Scholar 

  • Ruffin, N. E., Reed, B. L., Finnin, B. C.: The specificity of melatonin as a melanophore controlling factor in the pencil fish. Life Sci. 8, 1167–1174 (1969)

    Google Scholar 

  • Schäfer, O.: Spektrale Empfindlichkeit und absolute Schwelle des Farbwechsels geblendeter Elritzen (Phoxinus phoxinus L.). Biol. Zbl. 83, 47–66 (1964)

    Google Scholar 

  • Schnitzlein, H. N.: The habenula and the dorsal thalamus of some teleosts. J. comp. Neurol. 118, 225–266 (1962)

    Google Scholar 

  • Steyn, W., Webb, M.: The pineal complex in the fish, Labeo umbratus. Anat. Rec. 136, 79–85 (1960)

    Google Scholar 

  • Studnička, F. K.: Die Parietalorgane. In: Lehrbuch der vergleichenden mikroskopischen Anatomie der Wirbeltiere (Hrsg. A. Oppel), Teil V. Jena: Gustav Fischer 1905

    Google Scholar 

  • Tilney, F., Warren, L. F.: The morphology and evolutional significance of the pineal body. Amer. anat. Memoirs, vol. 9. Philadelphia: Wistar Institute 1919

    Google Scholar 

  • Tretjakoff, D.: Die Parietalorgane von Petromyzon fluviatilis. Z. wiss. Zool. 113, 1–112 (1915)

    Google Scholar 

  • Tyrer, N. M., Bell, E. M.: The intensification of cobalt filled neurone profiles using a modification of the Timm's sulphide-silver method. Brain Res. (in press)

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Author notes

  1. Leghesse Zerihun

    Present address: College of Agriculture, Haile Selassie University, Dire Dawa, Ethiopia

Authors and Affiliations

  1. School of Biological Sciences, University of Kentucky, Lexington, Kentucky, USA

    Mohammad A. Hafeez & Leghesse Zerihun

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  1. Mohammad A. Hafeez
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Additional information

Supported in part by grants to the senior author from the National Institute of Health (NS-10600) and the University of Kentucky Biomedical Science Support.—This paper is dedicated to Professor J. Ariëns Kappers and to the memory of Professor Nils Holmgren.

The authors wish to thank Dr. David Prior for his valuable assistance in the use of the cobalt technique; Dr. M. Tyrer for suggesting Timm's method; Dr. John Just for helpful suggestions and reading the manuscript, Mrs. Munira Nasser for histological preparations and other technical assistance.

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Hafeez, M.A., Zerihun, L. Studies on central projections of the pineal nerve tract in rainbow trout, Salmo gairdneri Richardson, using cobalt chloride iontophoresis. Cell Tissue Res. 154, 485–510 (1974). https://doi.org/10.1007/BF00219669

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