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Development of arginine vasotocin innervation in two species of anuran amphibian:Rana catesbeiana andRana sylvatica

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Abstract

Arginine vasotocin (AVT) is a neurotransmitter in the amphibian central nervous system and is released from the neurohypophysis in the regulation of hydromineral balance and other homeostatic functions. Many amphibians experience drastic changes in habitat with respect to water availability during their transformation from aquatic larvae to terrestrial adults. To examine whether metamorphosis is accompanied by a reorganization of central vasotocinergic neurons, the developmental organization of vasotocin neurons and nerve fibers was studied with immunocytochemistry in the brains of bullfrogs (Rana catesbeiana) and woodfrogs (R. sylvatica). In bullfrogs, early limb-bud-stage tadpoles had AVT-immunoreactive neurons and nerve fibers in the lateral septal nucleus, amygdala, preoptic hypothalamus, suprachiasmatic nucleus, and posterodorsal tegmentum. Woodfrog larvae showed similar patterns of hypothalamic AVT immunoreactivity, although neuronal staining in the amygdala did not appear until metamorphic climax, and never appeared in septal neurons or in the posterodorsal tegmentum. Whereas the highly terrestrialR. sylvatica adults must adapt to an adult habitat with prolonged periods of dehydration,R. catesbeiana adults remain semiaquatic and, as such, need not develop extreme mechanisms for water retention. Nonetheless, vasotocinergic pathways showed developmental similarities in the two species. The early appearance of AVT innervation in bothRana suggests that AVT has neuroregulatory functions well before metamorphosis.

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References

  • Alvarado RH, Johnson SR (1965) Effects of arginine vasotocin and oxytocin on sodium and water balance inAmbystoma. Comp Biochem Physiol 16:531–546

    Article  PubMed  Google Scholar 

  • Alvarado RH, Johnson SR (1966) The effects of neurohypophysial hormones on water and sodium balance in larval and adult bullfrogs (Rana catesbeiana). Comp Biochem Physiol 18:549–561

    Article  PubMed  Google Scholar 

  • Alvarado RH, Moody A (1970) Sodium and chloride transport in tadpoles of the bullfrogRana catesbeiana. Am J Physiol 218:1510–1516

    PubMed  Google Scholar 

  • Bentley PJ (1974) Actions of neurohypophysial hormones in amphibians, reptiles, and birds. In: Kobnil E, Sawyer WH (eds) Handbook of physiology, vol 4. American Physiological Socienty Bethesda, Md., pp 545–563

    Google Scholar 

  • Bentley PJ (1987) Actions of hormones on salt and water transport across cutaneous and urinary bladder epithelia. In: Pang PKT, Schreiberman MP (eds) Vertebrate endocrinology: fundamentals and biomedial implications regulation of water and electrolytes, vol 2. Academic Press, New York, pp 271–291

    Google Scholar 

  • Bentley PJ, Greenwald L (1970) Neurohypophysial function in bullfrog (Rana catesbeiana) tadpoles. Gen Comp Endocrinol 14:412–415

    Article  PubMed  Google Scholar 

  • Boyd SK (1994) Development of vasotocin pathways in the bullfrog brain. Cell Tissue Res 276:593–602

    PubMed  Google Scholar 

  • Boyd SK, Moore FL (1991) Gonadectomy reduces the concentrations of putative receptors for arginine vasotocin in the brain of an amphibian. Brain Res 541:193–197

    Article  PubMed  Google Scholar 

  • Boyd SK, Moore LF (1992) Sexually dimorphic concentrations of arginine vasotocin in sensory regions of the amphibian brain. Brain Res 588:304–306

    Article  PubMed  Google Scholar 

  • Boyd SK, Tyler CJ, De Vries GJ (1992) Sexual dimorphism in the vasotocin system of the bullfrog (Rana catesbeiana). J Comp Neurol 325:313–325

    Article  PubMed  Google Scholar 

  • Brown SC, Horgan EA, Savage LM, Brown PS (1986) Changes in body water and plasma constituents during bullfrog development. effects of temperature and hormone. J Exp Zool 237: 25–34

    PubMed  Google Scholar 

  • Buijs RM, Pévet P (1979) Vasopressin- and oxytocin-containing fibres in the pineal gland and subcommissural organ of the rat. Cell Tissue Res 205:11–17

    Google Scholar 

  • Carr JA, Norris DO (1990) Immunohistochemical localization of corticotropin-releasing factor and arginine vasotocin-like immunoreactivities in the brain and pituitary of the American bullfrog (Rana catesbeiana) during development and metamorphosis. Gen Comp Endocrinol 78:180–188

    Article  PubMed  Google Scholar 

  • Gonzalez A, Smeets W (1992) Comparative analysis of the vasotocinergic and mesotocinergic cells and fibers in the brain of two amphibians, the anuranRana ridibunda and the urodelePleurodeles waltlii. J Comp Neurol 315:53–73

    Article  PubMed  Google Scholar 

  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190

    Google Scholar 

  • Hillman SS (1974) The effect of arginine vasotocin on water and sodium balance in the urodele amphibianAneides luguburis. Gen Comp Physiol 24:74–82

    Google Scholar 

  • Iwamuro S, Hayashi H, Yamashita M, Kikuyama S (1991) Arginine vasotocin (AVT) and AVT-related peptide are major adlosterone-releasing factors in the bullfrog neurointermediate lobe. Gen Comp Physiol 84:412–418

    Google Scholar 

  • Jorgenson CB, Levi H, Zerahn K (1954) On active uptake of sodium and chloride ions in anurans. Acta Physiol Scand 30:178–190

    PubMed  Google Scholar 

  • Kar S, Naik DR (1978) Ontogeny of the hypothalamo-neurohypophysial system in the toad,Bufo melanostictus: an immunohistochemical study. Gen Comp Endocrinol 65:184–188

    Article  Google Scholar 

  • Lillywhite HB (1975) Physiological correlates of basking in amphibians. Comp Biochem Physiol 52A:323–330

    Article  Google Scholar 

  • Moore FL, Wood RE, Boyd SK (1992) Sex steroids and vasotocin interact in a female amphibian (Taricha granulosa) to elicit female-like egg-laying behaviour or male-like courtship. Horm Behav 26:156–166

    Article  PubMed  Google Scholar 

  • Nieuwenhuys R, Opdam P (1976) Structure of the brain stem. In: Llinas R, Precht W (eds) Frog neurobiology Springer Berlin Heidelberg New York, pp 811–855

    Google Scholar 

  • Northcutt RG, Ronan M (1992) Afferent and efferent connections of the bullfrog medial pallium. Brain Behav Evol 40:1–16

    PubMed  Google Scholar 

  • Pang PKT, Uchiyama M, Sawyer WH (1982) Endocrine and neural control of amphibian renal functions. Fed Proc 41:2365–2370

    PubMed  Google Scholar 

  • Satoh T, Endou H (1990) Inhibitory effect of phorbol ester on sodium transport in frog urinary bladder. Am J Physiol 259: F425-F431

    PubMed  Google Scholar 

  • Sawyer WH (1951) Effect of posterior pituitary extracts on urine formation and glomerular circulation in the frog. Am J Physiol 164:457–466

    PubMed  Google Scholar 

  • Sawyer WH (1957) Increased renal reabsorption of osmotically free water by the toad (Bufo marinus) in response to neurohypophysial hormones. Am J Physiol 189:564–568

    PubMed  Google Scholar 

  • Simmoneaux V, Ouichou A, Burbach JPH, Pévet P (1990) Vasopressin and oxytocin modulation of melatonin secretion from rat pineal glands. Peptides 11:1075–1079

    Article  PubMed  Google Scholar 

  • Sternberger LA, Hardy PH, Cuculis JJ, Meyers HG (1970) The unlabeled antibody enzyme method of immunocytochemistry preparation and properties of soluble antigen-antibody complex (horseradish peroxidase-antiperoxidase) and its use in identification of spirochetes. J Histochem Cytochem 18:315–333

    PubMed  Google Scholar 

  • Vandesande F, Dierickx K (1976) Immunocytochemical demonstration of separate vasotocinergic and mesotocinergic neurons in the amphibian hypothalamic magnocellular neurosecretory system. Cell Tissue Res 175:289–296

    Article  PubMed  Google Scholar 

  • Vivien-Roels B, Guerne JM, Holder FC, Schroeder MD (1979) Comparative immunohistochemical, radioimmunological and biological attempts to identify arginine-vasotocin (AVT) in the pineal gland of reptiles and fishes. Brain Res 52:459–463

    Google Scholar 

  • Warburg MR, Goldenberg S (1978) Effect of oxytocin and vasotocin on water balance in two urodeles followed throughout their life cycle. Comp Biochem Physiol 60:113–116

    Article  Google Scholar 

  • Wright AH, Wright AA (1949) Handbook of frogs and toads. Comstock Publishing Co

  • Zoeller RT, Moore FL (1986) Arginine vasotocin immunoreactivity in hypothalamic and extrahypothalamic areas of an amphibian brain. Neuroendocrinol 42:120–123

    Google Scholar 

  • Zoeller RT, Moore FL (1988a) Brain arginine vasotocin concentrations related to sexual behaviours and hydromineral balance in an amphibian. Horm Behav 22:66–75

    Article  PubMed  Google Scholar 

  • Zoeller RT, Moore FL (1988b) Correlation between immunoreactive vasotocin in the optic tectum and seasonal changes in reproductive behaviours of male rough-skinned newts. Horm Behav 20:148–154.

    Article  Google Scholar 

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Mathieson, W.B. Development of arginine vasotocin innervation in two species of anuran amphibian:Rana catesbeiana andRana sylvatica . Histochem Cell Biol 105, 305–318 (1996). https://doi.org/10.1007/BF01463933

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