Advertisement

Cell and Tissue Research

, Volume 353, Issue 3, pp 525–538 | Cite as

A candidate of organum vasculosum of the lamina terminalis with neuronal connections to neurosecretory preoptic nucleus in eels

  • Takao MukudaEmail author
  • Sawako Hamasaki
  • Yuka Koyama
  • Yoshio Takei
  • Toshiyuki Kaidoh
  • Takao Inoué
Regular Article

Abstract

Systemic angiotensin II (Ang II) is a dipsogen in terrestrial vertebrates and seawater teleosts. In eels, Ang II acts on the area postrema, a sensory circumventricular organ (CVO) and elicits water intake but other sensory CVOs have not yet been found in the eel forebrain. To identify sensory CVOs in the forebrain, eels were peripherally injected with Evans blue, which immediately binds to albumin, or a rabbit IgG protein. Extravasation of these proteins, which cannot cross the blood–brain barrier (BBB), was observed in the brain parenchyma of the anteroventral preoptic recess (PR) walls. Fenestrated capillaries were observed in the parenchymal margin of the ventral wall of the PR, confirming a deficit of the BBB in the eel forebrain. Immunostaining for tyrosine hydroxylase (TH) and choline acetyltransferase (ChAT) detected neurons in the lateral region of the anterior parvocellular preoptic nucleus (PPa), which were strongly stained by BBB-impermeable N-hydroxysulfosuccinimide. In the periventricular region of the PPa, many neurons incorporated biotinylated dextran amine conjugated to fluorescein, a retrograde axonal tracer, injected into the magnocellular preoptic nucleus (PM), indicating neuronal connections from the PPa to the PM. The mammalian paraventricular and supraoptic nuclei, homologous to the teleost PM, receive principal neuronal projections from the organum vasculosum of the lamina terminalis (OVLT). These results strongly suggest that the periventricular subpopulation of the PPa, which is most likely to be a component of the OVLT, serves as a functional window of access for systemic signal molecules such as Ang II.

Keywords

Vascular permeability Fenestrated capillary Sensory circumventricular organ Osmoregulation Water intake 

Notes

Acknowledgments

The authors thank Prof. Y. Furukawa (Hiroshima University) and Dr. M. Ando (The University of Tokyo) for valuable suggestions. This work was supported in part by a Grant-in-Aid for Scientific Research (A) (no. 23247010 to Takei Y) from JSPS.

References

  1. Amer S, Brown JA (1995) Glomerular actions of arginine vasotocin in the in situ perfused trout kidney. Am J Physiol 269:R775–R780PubMedGoogle Scholar
  2. Anadón R, Molist P, Rodríguez-Moldes I, López JM, Quintela I, Cerviño MC, Barja P, González A (2000) Distribution of choline acetyltransferase immunoreactivity in the brain of anelasmobranch, the lesser spotted dogfish (Scyliorhinus canicula). J Comp Neurol 420:139–170PubMedCrossRefGoogle Scholar
  3. Ando M, Fujii Y, Kadota T, Kozaka T, Mukuda T, Takase I, Kawahara A (2000) Some factors affecting drinking behavior and their interactions in seawater-acclimated eels, Anguilla japonica. Zool Sci 17:171–178CrossRefGoogle Scholar
  4. Anglade I, Zandbergen T, Kah O (1993) Origin of the pituitary innervation in the goldfish. Cell Tissue Res 273:345355CrossRefGoogle Scholar
  5. Arenzana FJ, Clemente D, Sánchez-González R, Porteros A, Aijón J, Arévalo R (2005) Development of the cholinergic system in the brain and retina of the zebrafish. Brain Res Bull 66:421–425PubMedCrossRefGoogle Scholar
  6. Babiker MM, Rankin JC (1978) Neurohypophysial hormonal control of kidney function in the European eel (Anguilla anguilla L.) adapted to sea-water or fresh water. J Endocrinol 76:347–358PubMedCrossRefGoogle Scholar
  7. Balment RJ, Lu W, Weybourne E, Warne JM (2006) Arginine vasotocin a key hormone in fish physiology and behaviour: a review with insights from mammalian models. Gen Comp Endocrinol 147:9–16PubMedCrossRefGoogle Scholar
  8. Barreiro-Iglesias A, Villar-Cerviño V, Villar-Cheda B, Anadón R, Rodicio MC (2008) Neurochemical characterization of sea lamprey taste buds and afferent gustatory fibers: presence of serotonin, calretinin, and CGRP immunoreactivity in taste bud bi-ciliated cells of the earliest vertebrates. J Comp Neurol 511:438–453PubMedCrossRefGoogle Scholar
  9. Bond H, Winter MJ, Warne JM, McCrohan CR, Balment RJ (2002) Plasma concentrations of arginine vasotocin and urotensin II are reduced following transfer of the euryhaline flounder (Platichthys flesus) from seawater to fresh water. Gen Comp Endocrinol 125:113–120PubMedCrossRefGoogle Scholar
  10. Canosa LF, Lopez GC, Scharrig E, Lesaux-Farmer K, Somoza GM, Kah O, Trudeau VL (2011) Forebrain mapping of secretoneurin-like immunoreactivity and its colocalization with isotocin in the preoptic nucleus and pituitary gland of goldfish. J Comp Neurol 519:3748–3765PubMedCrossRefGoogle Scholar
  11. Castro A, Becerra M, Anadón R, Manso MJ (2008) Distribution of calretinin during development of the olfactory system in the brown trout, Salmo trutta fario: Comparison with other immunohistochemical markers. J Chem Neuroanat 35:306–316PubMedCrossRefGoogle Scholar
  12. Clemente D, Porteros A, Weruaga E, Alonso JR, Arenzana FJ, Aijón J, Arévalo R (2004) Cholinergic elements in the zebrafish central nervous system: histochemical and immunohistochemical analysis. J Comp Neurol 474:75–107PubMedCrossRefGoogle Scholar
  13. Cottrell GT, Ferguson AV (2004) Sensory circumventricular organs: central roles in integrated autonomic regulation. Regul Pept 117:11–23PubMedCrossRefGoogle Scholar
  14. De Luca LA, Jr XZ, Schoorlemmer GH, Thunhorst RL, Beltz TG, Menani JV, Johnson AK (2002) Water deprivation-induced sodium appetite: humoral and cardiovascular mediators and immediate early genes. Am J Physiol Regul Integr Comp Physiol 282:R552–R559PubMedGoogle Scholar
  15. Finger TE, Kanwal JS (1992) Ascending general visceral pathways within the brainstems of two teleost fishes: Ictalurus punctatus and Carassius auratus. J Comp Neurol 320:509–520PubMedCrossRefGoogle Scholar
  16. Fitzsimons JT (1998) Angiotensin, thirst, and sodium appetite. Physiol Rev 78:583–686PubMedGoogle Scholar
  17. Folgueira M, Anadón R, Yáñez J (2003) Experimental study of the connections of the gustatory system in the rainbow trout, Oncorhynchus mykiss. J Comp Neurol 465:604–619PubMedCrossRefGoogle Scholar
  18. Gómez-Segade P, Segade LA, Anadón R (1991) Ultrastructure of the organum vasculosum laminae terminalis in the advanced teleost Chelon labrosus (Risso, 1826). J Hirnforsch 32:69–77PubMedGoogle Scholar
  19. Greenwood AK, Wark AR, Fernald RD, Hofmann HA (2008) Expression of arginine vasotocin in distinct preoptic regions is associated with dominant and subordinate behaviour in an African cichlid fish. Proc R Soc Lond B 275:2393–2402CrossRefGoogle Scholar
  20. Haruta K, Yamashita T, Kawashima S (1991) Changes in arginine vasotocin content in the pituitary of the Medaka (Oryzias latipes) during osmotic stress. Gen Comp Endocrinol 83:327–336PubMedCrossRefGoogle Scholar
  21. Holmqvist BI, Ekström P (1995) Hypophysiotrophic systems in the brain of the Atlantic salmon. Neuronal innervation of the pituitary and the origin of pituitary dopamine and nonapeptides identified by means of combined carbocyanine tract tracing and immunocytochemistry. J Chem Neuroanat 8:125–145PubMedCrossRefGoogle Scholar
  22. Jeong JY, Kwon HB, Ahn JC, Kang D, Kwon SH, Park JA, Kim KW (2008) Functional and developmental analysis of the blood–brain barrier in zebrafish. Brain Res Bull 75:619–628PubMedCrossRefGoogle Scholar
  23. Johnson AK, Gross PM (1993) Sensory circumventricular organs and brain homeostatic pathways. FASEB J 7:678–686PubMedGoogle Scholar
  24. Kah O, Dulka JG, Dubourg P, Thibault J, Peter RE (1987) Neuroanatomical substrate for the inhibition of gonadotrophin secretion in goldfish: existence of a dopaminergic preoptico-hypophyseal pathway. Neuroendocrinology 45:451–458PubMedCrossRefGoogle Scholar
  25. Kawamoto K, Kawashima S (1986) Effects of glucocorticoids and vasopressin on the regeneration of neurohypophyseal hormonecontaining axons after hypophysectomy. Zool Sci 3:723–726Google Scholar
  26. Kobayashi H, Takei Y (1996) The renin-angiotensin system: comparative aspect. Zoophysiology, vol 35. Springer, BerlinCrossRefGoogle Scholar
  27. Kozaka T, Fujii Y, Ando M (2003) Central effects of various ligands on drinking behavior in eels acclimated to seawater. J Exp Biol 206:687–692PubMedCrossRefGoogle Scholar
  28. Linard B, Anglade I, Corio M, Navas JM, Pakdel F, Saligaut C, Kah O (1996) Estrogen receptors are expressed in a subset of tyrosine hydroxylase-positive neurons of the anterior preoptic region in the rainbow trout. Neuroendocrinology 63:156–165PubMedCrossRefGoogle Scholar
  29. Ma PM (1994) Catecholaminergic systems in the zebrafish. I. Number, morphology, and histochemical characteristics of neurons in the locus coeruleus. J Comp Neurol 344:242–255PubMedCrossRefGoogle Scholar
  30. Montero M, Vidal B, King JA, Tramu G, Vandesande F, Dufour S, Kah O (1994) Immunocytochemical localization of mammalian GnRH (gonadotropin-releasing hormone) and chicken GnRH-II in the brain of the European silver eel (Anguilla anguilla L.). J Chem Neuroanat 7:227–241PubMedCrossRefGoogle Scholar
  31. Mueller T, Vernier P, Wullimann MF (2004) The adult central nervous cholinergic system of a neurogenetic model animal, the zebrafish Danio rerio. Brain Res 1011:156–169PubMedCrossRefGoogle Scholar
  32. Mukuda T, Ando M (2003a) Medullary motor neurones associated with drinking behaviour of Japanese eels. J Fish Biol 62:1–12CrossRefGoogle Scholar
  33. Mukuda T, Ando M (2003b) Brain atlas of the Japanese eel: Comparison to other fishes. Mem Fac Integr Arts Sci Hiroshima Univ Ser IV 29:1–25Google Scholar
  34. Mukuda T, Ando M (2010) Central regulation of the pharyngeal and upper esophageal reflexes during swallowing in the Japanese eel. J Comp Physiol A 196:111–122CrossRefGoogle Scholar
  35. Mukuda T, Matsunaga Y, Kawamoto K, Yamaguchi K, Ando M (2005) “Blood-contacting neurons” in the brain of the Japanese eel Anguilla japonica. J Exp Zool 303:366–376CrossRefGoogle Scholar
  36. Nobata S, Takei Y (2011) The area postrema in hindbrain is a central player for regulation of drinking behavior in Japanese eels. Am J Physiol Regul Integr Comp Physiol 300:R1569–R1577PubMedCrossRefGoogle Scholar
  37. Oldfield BJ, Bicknell RJ, McAllen RM, Weisinger RS, McKinley MJ (1991) Intravenous hypertonic saline induces Fos immunoreactivity in neurons throughout the lamina terminalis. Brain Res 561:151–156PubMedCrossRefGoogle Scholar
  38. Pérez SE, Yáñez J, Marín O, Anadón R, González A, Rodríguez-Moldes I (2000) Distribution of choline acetyltransferase (ChAT) immunoreactivity in the brain of the adult trout and tract-tracing observations on the connections of the nuclei of the isthmus. J Comp Neurol 428:450–474PubMedCrossRefGoogle Scholar
  39. Pombal MA, Marín O, González A (2001) Distribution of choline acetyltransferase-immunoreactive structures in the lamprey brain. J Comp Neurol 431:105–126PubMedCrossRefGoogle Scholar
  40. Pombal MA, Abalo XM, Rodicio MC, Anadón R, González A (2003) Choline acetyltransferase-immunoreactive neurons in the retina of adult and developing lampreys. Brain Res 993:154–163PubMedCrossRefGoogle Scholar
  41. Roberts BL, Meredith GE, Maslam S (1989) Immunocytochemical analysis of the dopamine system in the brain and spinal cord of the European eel, Anguilla anguilla. Anat Embryol (Berl) 180:401–412CrossRefGoogle Scholar
  42. Saito D, Komatsuda M, Urano A (2004) Functional organization of preoptic vasotocin and isotocin neurons in the brain of rainbow trout: central and neurohypophysial projections of single neurons. Neuroscience 124:973–984PubMedCrossRefGoogle Scholar
  43. Sueiro C, Carrera I, Rodríguez-Moldes I, Molist P, Anadón R (2003) Development of catecholaminergic systems in the spinal cord of the dogfish Scyliorhinus canicula (Elasmobranchs). Brain Res Dev Brain Res 142:141–150PubMedCrossRefGoogle Scholar
  44. Takei Y (2000) Comparative physiology of body fluid regulation in vertebrates with special reference to thirst regulation. Jpn J Physiol 50:171–186PubMedCrossRefGoogle Scholar
  45. Takei Y, Hirano T, Kobayashi H (1979) Angiotensin and water intake in the Japanese eel, Anguilla japonica. Gen Comp Endocrinol 38:466–475PubMedCrossRefGoogle Scholar
  46. Teitsma CA, Anglade I, Lethimonier C, Le Drean G, Saligaut D, Ducouret B, Kah O (1999) Glucocorticoid receptor immunoreactivity in neurons and pituitary cells implicated in reproductive functions in rainbow trout: a double immunohistochemical study. Biol Reprod 60:642–650PubMedCrossRefGoogle Scholar
  47. Tsukada T, Nobata S, Hyodo S, Takei Y (2007) Area postrema, a brain circumventricular organ, is the site of antidipsogenic action of circulating atrial natriuretic peptide in eels. J Exp Biol 210:3970–3978PubMedCrossRefGoogle Scholar
  48. Tsuneki K (1986) A survey of occurrence of about seventeen circumventricular organs in brains of various vertebrates with special reference to lower groups. J Hirnforsch 27:441–470PubMedGoogle Scholar
  49. Uyama O, Okamura N, Yanase M, Narita M, Kawabata K, Sugita M (1988) Quantitative evaluation of vascular permeability in the gerbil brain after transient ischemia using Evans blue fluorescence. J Cereb Blood Flow Metab 8:282–284PubMedCrossRefGoogle Scholar
  50. Warne JM, Balment RJ (1997) Changes in plasma arginine vasotocin (AVT) concentration and dorsal aortic blood pressure following AVT injection in the teleost Platichthys flesus. Gen Comp Endocrinol 105:358–364PubMedCrossRefGoogle Scholar
  51. Warne JM, Bond H, Weybourne E, Sahajpal V, Lu W, Balment (2005) Altered plasma and pituitary arginine vasotocin and hypothalamic provasotocin expression in flounder (Platichthys flesus) following hypertonic challenge and distribution of vasotocin receptors within the kidney. Gen Comp Endocrinol 44:240–247CrossRefGoogle Scholar
  52. Weltzien FA, Pasqualini C, Sébert ME, Vidal B, Le Belle N, Kah O, Vernier P, Dufour S (2006) Androgen-dependent stimulation of brain dopaminergic systems in the female European eel (Anguilla anguilla). Endocrinology 147:2964–2973PubMedCrossRefGoogle Scholar
  53. Yamada C, Noji S, Shioda S, Nakai Y, Koayashi H (1990) Intragranular colocalization of arginine vasopressin- and angiotensin II-like immunoreactivity in the hypothalamo-neurohypophysial system of the goldfish, Carassius auratus. Zool Sci 7:257–263Google Scholar
  54. Zucker DK, Wooten GF, Lothman EW (1983) Blood–brain barrier changes with kainic acid-induced limbic seizures. Exp Neurol 79:422–433PubMedCrossRefGoogle Scholar
  55. Zupanc GK (1998) An in vitro technique for tracing neuronal connections in the teleost brain. Brain Res Protocol 3:37–51CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Takao Mukuda
    • 1
    Email author
  • Sawako Hamasaki
    • 2
  • Yuka Koyama
    • 2
  • Yoshio Takei
    • 3
  • Toshiyuki Kaidoh
    • 4
  • Takao Inoué
    • 5
  1. 1.Laboratory of Integrative Physiology, Graduate School of Integrated Arts & SciencesHiroshima UniversityHigashi-hiroshimaJapan
  2. 2.Laboratory of Neurobiology, Graduate School of Integrated Arts & SciencesHiroshima UniversityHiroshimaJapan
  3. 3.Laboratory of Physiology, Atmosphere and Ocean Research InstituteThe University of TokyoChibaJapan
  4. 4.Division of Medical Morphology, Department of AnatomyTottori University Faculty of MedicineTottoriJapan
  5. 5.Division of Morphological Analysis, Department of AnatomyTottori University Faculty of MedicineTottoriJapan

Personalised recommendations