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Organization of the serotoninergic system in the brain of two amphibian species, Ambystoma mexicanum (Urodela) and Typhlonectes compressicauda (Gymnophiona)

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Abstract

An immunocytochemical investigation was made of the distribution of serotonin (5-HT) in the brain of larval and adult Ambystoma mexicanum and adult Typhlonectes compressicauda. Immunoreactive perikarya can be identified in the caudal diencephalon (paraventricular organ and infundibular nucleus), in the ventral mesencephalon (interpeduncular nucleus) and in the raphe of the rhombencephalon. Immunopositive fibers and terminal arborizations are widely distributed, extending from the whole telencephalon to the spinal lemniscus area. However, the retinorecipient structures of the thalamus and mesencephalon are either very weakly innervated (Ambystoma) or completely immunonegative (Typhlonectes). The habenular system also exhibits very few 5-HT-positive structures. The major serotoninergic neuron clusters, in both Urodela and Gymnophiona, tend to gather, from the paraventricular organ to the raphe, on both sides of the sagittal plane, showing no tendency to “lateralization”. A new interpretation of the limited development of the serotoninergic system in amphibians is given.

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References

  • Azmitia EC, Segal M (1978) An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J Comp Neurol 179:641–659

    Google Scholar 

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

    Google Scholar 

  • Beltramo M, Krieger M, Calas A, Franzoni MF, Thibault J (1993) Aromatic amino acid decarboxylase (AADC) immunohistochemistry in the vertebrate brainstem with an antiserum raised against AADC made in E. coli Brain Res Bull 32:123–132

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Capanna E, Clairambault P (1974) Neuronal typology in the anuran telencephalon: a Golgi study. Acta Anat 89:321–332

    Google Scholar 

  • Chacko T, Terlou M, Peute J (1974) Fluorescence and electron microscopical study of aminergic nuclei in the brain of Bufo poweri. Cell Tissue Res 149:481–495

    Google Scholar 

  • Challet E, Pierre J, Repérant J, Ward R, Miceli D (1991) The serotoninergic system of the brain of the viper, Vipera aspis. An immunohistochemical study. J Chem Neuroanat 4:233–248

    Google Scholar 

  • Clairambault P, Cordier-Picouet MJ, Pairault C (1980) Premières données sur les projections visuelles d'un Amphibien Apode (Typhlonectes compressicauda). C R Acad Sci III 291:283–286

    Google Scholar 

  • Corio M, Doerr-Schott J (1988) The monoaminergic system in the diencephalon of the newt tadpole Triturus alpestris. A histofluorescence study. J Hirnforsch 29:377–384

    Google Scholar 

  • Corio M, Peute J, Steinbush HWM (1991) Distribution of serotonin- and dopamin-immunoreactivity in the brain of the teleost Clarias gariepinus. J Chem Neuroanat 4:79–95

    Google Scholar 

  • Corio M, Thibault J, Peute J (1992) Distribution of cathecholaminergic and serotoninergic systems in forebrain and midbrain of the newt, Triturus alpestris (Urodela). Cell Tissue Res 268:377–387

    Google Scholar 

  • Dalhström A, Fuxe K (1964) Evidence for the existence of monoamine-containing neurons in the central nervous system. I. Demonstration of monoamines in cell bodies of brain neurons. Acta Physiol Scand 62:1–55

    Google Scholar 

  • Dubé L, Parent A (1982) The organization of monoamine-containing neurons in the brain of the salamander Necturus maculosus. J Comp Neurol 211:21–30

    Google Scholar 

  • Dubé L, Clairambault P, Malacarne G (1990) Striatal afferents in the newt Triturus cristatus. Brain Behav Evol 35:212–226

    Google Scholar 

  • Duellman WE, Trueb L (1986) Biology of amphibians. McGraw-Hill, New York

    Google Scholar 

  • Ekström P, Ebbesson SOE (1988) The left habenular nucleus contains a discrete serotonin-immunoreactive subnucleus in the coho salmon (Oncorhynchus kisutch). Neurosci Lett 91:121–125

    Google Scholar 

  • Ekström P, Veen T van (1984) Distribution of 5-hydroxytryptamine (serotonin) in the brain of the teleost Gasterosteus acculeatus. J Comp Neurol 226:307–320

    Google Scholar 

  • Fasolo A, Franzoni MF, Gaudino G, Steinbusch HWM (1986) The organization of serotonin-immunoreactive neuronal systems in the brain of the crested newt Triturus cristatus carnifex Laur. Cell Tissue Res 243:239–247

    Google Scholar 

  • Frankenhuis-van den Heuvel THM, Nieuwenhuys R (1984) Distribution of serotonin-immunoreactivity in the diencephalon and the mesencephalon of the trout Salmo gairdneri: cell bodies, fibers and terminals. Anat Embryol 169:193–204

    Google Scholar 

  • Fritzsch B, Himstedt W, Crapon de Caprona M.D. (1985). Visual projections in larval Ichthyophis kohtaoensis (Amphibia Gymnophiona). Dev Brain Res 23:201–210

    Google Scholar 

  • Gonzales A, Smeets WJAJ (1991) Comparative analysis of dopamine and tyrosine hydroxylase immunoreactivities in the brain of two amphibians, the anuran Rana ridibunda and the urodele Pleurodeles waltlii. J Comp Neurol 303:457–477

    Google Scholar 

  • Gonzales A, Tuinhof R, Smeets WJAJ (1993) Distribution of tyrosine hydroxylase and dopamine immunoreactivities in the brain of the South African clawed frog Xenopus laevis. Anat Embryol 187:193–201

    Google Scholar 

  • Grant K, Clausse S, Libouban S, Szabo T (1989) Serotoninergic neurons in the mormyrid brain and their projections to preelectromotor and primary electrosensory centers: an immunohistochemical study. J Comp Neurol 281:114–128

    Google Scholar 

  • Hassler R (1978) Striatal control of locomotion, intentional actions and of integrative and perceptive activity. J Neurol Sci 36:187–224

    Google Scholar 

  • Himstedt W, Manteuffel G (1985) Retinal projections in the caecilian Ichthyophis kohtaoensis (Amphibia, Gymnophiona). Cell Tissue Res 239:689–692

    Google Scholar 

  • Jakway JS, Riss W (1972) Retinal projections in the tiger salamander, Ambystoma tigrinum. Brain Behav Evol 5:401–442

    Google Scholar 

  • Johnston SA, Maler L, Tinner B (1990) The distribution of serotonin in the brain of Apteronotus leptorhynchus: an immunohistochemical study. J Chem Neuroanat 4:429–465

    Google Scholar 

  • Kah O, Chambolle P (1983) Serotonin in the brain of the goldfish Carassius auratus. An immunocytochemical study. Cell Tissue Res 234:319–333

    Google Scholar 

  • Kemali M, Guglielmotti V (1971) An electron microscope observation of the right and left habenular nuclei of the frog. J Comp Neurol 176:133–148

    Google Scholar 

  • Kemali M, Lazar G (1985) Cobalt injected into the right and left fasciculi retroflexes clarifies the organization of this pathway. J Comp Neurol 233:1–11

    Google Scholar 

  • Kosaka T, Nagatsu I, Wu JY, Kama K (1986) Use of high concentrations of glutaraldehyde for immunocytochemistry of transmitter-synthesizing enzymes in the central nervous system. Neuroscience 18:975–990

    Google Scholar 

  • Kuhlenbeck H (1922) Zur Morphologie des Gymnophionengehirns. Jena Z Naturwiss 58:453–484

    Google Scholar 

  • Kuhlenbeck H, Malewitz TD, Beasley AB (1967) Further observations on the morphology of the forebrain in gymnophiona, with reference to the topologic vertebrate forebrain pattern. In: Hassler R, Stephan H (eds) Evolution of the forebrain. Plenum Press, New York, pp 9–19

    Google Scholar 

  • Larsell O (1967) The comparative anatomy and histology of the cerebellum, from Myxinoids through birds. Jansen J (ed) University of Minnesota Press, Minneapolis

    Google Scholar 

  • Lavoie B, Parent A (1991) Serotoninergic innervation of the thalamus in the primate: an immunohistochemical study. J Comp Neurol 312:1–18

    Google Scholar 

  • Linke R, Roth G, Rottluff B (1986) Comparative studies on the eye morphology of lungless salamander, family Plethodontidae, and the effect of miniaturization. J Morphol 189:131–143

    Google Scholar 

  • Malacarne G, Vellano C (1982) Effects of nostrils plugging and habenulectomy on sexual behaviour in the male crested newt. Behav Processes 7:307–317

    Google Scholar 

  • Meek J, Joosten HWH (1989) Distribution of serotonin in the brain of the mormyrid teleost Gnathonemus petersii. J Comp Neurol 281:206–224

    Google Scholar 

  • Nakai Y, Ochiai H, Shioda S, Ochi J (1977) Cytological evidence for different types of cerebrospinal fluid-contacting subependymal cells in the preoptic and infundibular recess of the frog. Cell Tissue Res 176:317–334

    Google Scholar 

  • Northcutt RG, Kicliter E (1980) Organization of the amphibian telencephalon. In: Ebbesson SOE (ed) Comparative neurology of the telencephalon. Plenum Press, New York, pp 203–251

    Google Scholar 

  • Opdam P, Nieuwenhuys R (1976) Topographical analysis of the brain stem of the Axolotl Ambystoma mexicanum. J Comp Neurol 165:285–306

    Google Scholar 

  • Pairault C, Christophe N, Faivre MN, Clairambault P (1993) Developmental organization of catecholaminergic and serotoninergic structures in the brain of a neotenic amphibian, Ambystoma mexicanum. Eur J Neurosci [Suppl 6] 164

  • Parent A (1973) Distribution of monoamine-containing neurons in the brainstem of the frog Rana temporaria. J Morphol 139:67–78

    Google Scholar 

  • Parent A (1975) The monoaminergic innervation of the telencephalon of the frog Rana pipiens. Brain Res 99:35–47

    Google Scholar 

  • Parent A (1984) Functional anatomy and evolution of monoaminergic system. Am Zool 24:783–790

    Google Scholar 

  • Pierre J, Repérant J, Ward R, Vesselkin NP, Rio J-P, Miceli D, Kratskin I (1992) The serotoninergic system of the brain of the Lamprey, Lampetra fluviatilis: an evolutionary perspective. J Chem Neuroanat 5:195–219

    Google Scholar 

  • Prasada Rao PD, Hartwig HG (1974) Monoaminergic tracts of the diencephalon and innervation of the pars intermedia in Rana temporaria. A fluorescence and microspectrofluorimetric study. Cell Tissue Res 151:1–26

    Google Scholar 

  • Sano Y, Ueda S, Yamada H, Takeuchi Y, Goto M, Kawata M (1983) Immunohistochemical demonstration of serotonin containing CSF-contacting neurons in the submammalian paraventricular organ. Histochemistry 77:423–430

    Google Scholar 

  • Sassoè-Pognetto M, Pairault C, Clairambault P, Fasolo A (1991) The connections of the anterior pallium in Pleurodeles Waltl and Triturus carnifex: an HRP study. J Hirnforsch 32:397–407

    Google Scholar 

  • Shimizu K, Kimura H, Ochi J (1983) Immunohistochemical demonstration of serotonin-containing subependymal cells in the frog hypothalamus. Histochemistry 79:23–29

    Google Scholar 

  • Smeets WJAJ, Steinbusch HWM (1988) Distribution of serotonin immunoreactivity in the forebrain and midbrain of the Lizard Gekko gecko. J Comp Neurol 271:419–434

    Google Scholar 

  • Stuesse SL, Cruce WLR, Northcutt RG (1990) Distribution of tyrosine hydroxylase- and serotonin-immunoreactive cells in the central nervous system of the thornback guitarfish, Platyrhinoides tsiseriata. J Chem Neuroanat 3:45–58

    Google Scholar 

  • Stuesse SL, Cruce WLR, Northcutt RG (1991) Localization of serotonin, tyrosine hydroxylase and leu-enkephalin immunoreactive cells in the brainstem of the horn Shark, Heterodontus francisci. J Comp Neurol 308:277–292

    Google Scholar 

  • Tan H, Miletic V (1990) Bulbospinal serotoninergic pathways in the frog Rana pipiens. J Comp Neurol 292:291–302

    Google Scholar 

  • Terlou M, Ploemacher RE (1973) The distribution of monoamines in the tel-, di- and mesencephalon of Xenopus laevis tadpoles, with special reference to the hypothalamo-hypophyseal system. Z Zellforsch Mikrosk Anat 137:521–540

    Google Scholar 

  • Timmel JF (1989) Dissymétrie habénulaire au cours de l'ontogenèse chez Pleurodeles waltl. J Hirnforsch 30:249–256

    Google Scholar 

  • Timmel JF, Clairambault P (1988) Premières données sur la mise en place des connexions habénulaires au cours du développement chez Pleurodeles. C R Acad Sci III 306:507–510

    Google Scholar 

  • Ueda S, Noiyo Y, Sano Y (1984) Immunohistochemical demonstration of serotonin neurons in the central nervous system of the bullfrog Rana catesbeiana. Anat Embryol 169:219–229

    Google Scholar 

  • Vigh-Teichmann I, Vigh B, Koritsansky S (1970) Liquorkontaktneurone im Nucleus paraventricularis. Z Zellforsch Mikrosk Anat 103:483–501

    Google Scholar 

  • Wake MH (1985) The comparative morphology and evolution of the eyes of Coecilians (Amphibia, Gymnophiona). Zoomorphology 105:277–295

    Google Scholar 

  • Wiechmann AF, Wirsig-Wiechmann CR (1993) Distribution of melatonin receptors in the brain of the frog Rana pipiens as revealed by in vitro autoradiography. Neuroscience 52:469–480

    Google Scholar 

  • Yoshida M, Nagatsu I, Kwakami-Kondo Y, Karasawa N, Spatz M, Nagatsu T (1983) Monoaminergic neurons in the brain of the goldfish as observed by immunohistochemical techniques. Experientia 39:1171–1174

    Google Scholar 

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Clairambault, P., Christophe, N., Pairault, C. et al. Organization of the serotoninergic system in the brain of two amphibian species, Ambystoma mexicanum (Urodela) and Typhlonectes compressicauda (Gymnophiona). Anat Embryol 190, 87–99 (1994). https://doi.org/10.1007/BF00185849

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