Summary
Antibodies against serotonin and 5-methoxytryptamine reveal indolaminergic neurons innervating the proximal part of the efferent arterial vasculature, the filament epithelia, the central venous sinus, and certain other serotonergic cells of the teleost gill filament. In the same area, acetylcholinesterase-positive and indoleaminergic neurons have already been described. We propose that these populations of neurons belong to a single neuronal type but express different agents. Our current results support this idea; in particular, they point to the presence of a single type of serotonin-containing nerve terminal, impinging on vascular smooth muscle. These results are in agreement with physiological data showing (i) the existence of non-cholinergic (atropine-resistant) vasoconstriction of the gill vasculature after nerve stimulation, and (ii) a potent vasoconstrictory action of infused serotonin. In addition, the above-mentioned serotonergic neurons have synaptic contacts with catecholaminergic nerve fibers, suggesting the existence of a modulatory relationship between the sympathetic and the cranial autonomic nerves supplying the teleost gill. Finally, these neurons show morphological relationships with a previously undescribed type of branchialserotonergic cell. The role of the parasympathetic nerve plexus of the teleost gill filament in the control of respiration and ionoregulation is discussed.
Similar content being viewed by others
References
Bailly Y (1983) Recherches sur quelques innervations de la branchie des poissons. Thèse de 3eme cycle de cytologie, Université Pierre et Marie Curie, Paris
Bailly Y, Dunel-Erb S (1986) The sphincter of the efferent filament artery in teleost gills. I. Structure and parasympathetic innervation. J Morphol 187:219–237
Baumgarten HG, Björklund A, Lachenmayer L, Nobin A, Rosengren E (1973) Evidence for the existence of serotonin-, dopamine- and noradrenaline-containing neurons in the gut of Lampetra fluviatilis. Cell Tissue Res 141:33–54
Berridge MJ, Schlue WR (1978) Ion-selective electrode studies on the effects of 5-hydroxytryptamine on the intracellular level of potassium in an insect gland. J Exp Biol 78:203–216
Booth JH (1979a) The effects of oxygen supply, epinephrine and acetylcholine on the distribution of blood flow in trout gills. J Exp Biol 83:31–39
Booth JH (1979b) Circulation in trout gills: The relationship between branchial perfusion and the width of the lamellar blood space. Can J Zool 57:2183–2185
Boyd JD (1936) Nerve supply to the branchial arch arteries of vertebrates. J Anat 71:157–158
Dalton T (1979) Pharmacology of 5-hydroxytryptamine receptor in frog skin epithelium. Br J Pharmacol 65:579–585
Daxboeck C, Holeton GF (1978) Oxygen receptors in the rainbow trout Salmo gairdneri. Can J Zool 56:1254–1259
Dietz TH, Steffens WL, Kays WT, Silverman H (1985) Serotonin localization in the gills of the freshwater mussel Ligumia subrostrata. Can J Zool 63:1237–1243
Donald JA (1984) Adrenergic innervation of the gills of brown and rainbow trout, Salmo trutta and S gairdneri. J Morphol 182:307–316
Donald JA (1987) Comparative study of the adrenergic innervation of the teleost gill. J Morphol 193:63–73
Donowitz M, Charney AN, Asarkof N (1980) Effect of serotonin on active electrolyte transport in rabbit ileum, gall bladder and colon. Am J Physiol 239:G463–472
Dunel S, Laurent P (1977) Physiologie comparée: La vascularisation branchiale chez l'Anguille: Action de l'acétylcholine et de l'adrénaline sur la répartition d'une résine polymérisable dans les différents compartiments vasculaires. CR Acad Sci, Paris 284:2011–2014
Dunel S, Laurent P (1980) Functional organization of the gill vasculature in different classes of fish. In: Lahlou B (ed) Epithelial transport in the lower vertebrates. Cambridge Univ. Press, Cambridge, pp 37–58
Dunel-Erb S, Bailly Y (1986) The sphincter of the efferent filament artery in teleost gills. II. Sympathetic innervation. J Morphol 187:239–246
Dunel-Erb S, Bailly Y (1987) Smooth muscles in relation to the gill skeleton of Perca fluviatilis: organization and innervation. Cell Tissue Res 247:339–350
Dunel-Erb S, Bailly Y, Laurent P (1982) Neuroepithelial cells in fish gill primary lamellae. J Appl Physiol: Resp Env Ex Physiol 53:1342–1353
Dunel-Erb S, Bailly Y, Laurent P (1989) Neurons controlling the gill vasculature in five species of teleosts. Cell Tissue Res 255:567–573
Falck B, Owman C (1965) A detailed methodological description of the fluorescence method for the demonstration of biogenic amines. Acta Univ Lund Sect 27:1–23
Farrel AP (1980a) Vascular pathways in the gill of lingcod Ophiodon elongatus. Can J Zool 58:796–806
Farrel AP (1980b) Gill morphometrics, vessel dimensions and vascular resistance in lingcod Ophiodon elongatus. Can J Zool 58:807–818
Farrel AP (1981) Cardiovascular changes in the lingcod Ophiodon elongatus following adrenergic and cholinergic drug infusion. J Exp Biol 91:293–305
Farrel AP, Daxboeck C, Randall DJ (1979) The effect of input pressure and flow on the pattern and resistance to flow in the isolated perfused gill of a teleost fish. J Comp Physiol 133:233–240
Farrel AP, Sobin SS, Randall DJ, Crosby S (1980) Intralamellar blood flow patterns in fish gills. Am J Physiol 239:R428-R436
Geffard M (1985) Contribution à une approche immunologique des molécules neuro-informatives. Thèse Univ Bordeaux
Geffard M, Dulluc J, Rock A-M (1985) Antisera against the indolalkylamines: tryptophan, 5-hydroxytryptophan, 5-hydroxytryptamine, 5-methoxytryptophan and 5-methoxytryptamine tested by an enzyme-linked immunosorbent assay method. J Neurochem 44:1221–1228
Gershon MD (1982) Serotonergic neurotransmission in the gut. Scand J Gastroenterol 17 [Suppl] 71:27–41
Gershon MD, Sherman DL (1987) Noradrenergic innervation of serotonergic neurons in the myenteric plexus. J Comp Neurol 259:193–210
Gibbins IL (1982) Lack of correlation between ultrastructural and pharmacological types of non adrenergic autonomic nerves. Cell Tissue Res 221:551–581
Hökfelt T, Fuxe K, Goldstein M (1975) Applications of immunohistochemistry to studies on monoamine cell systems with special references to nervous tissue. Ann NY Acad Sci 254:407–432
Holbert PW, Boland EJ, Olson KR (1979) The effect of epinephrine and acetylcholine on the distribution of red cells within the gills of the channel catfish Ictalurus melas. J Exp Biol 79:135–146
Holeton GF (1977) Constancy of arterial pH during CO-induced hypoxia in the rainbow trout. Can J Zool 55:1010–1013
Hughes GM (1972) Morphometrics of fish gills. Respir Physiol 14:1–25
Katchen MS, Olson KR, Wayne C (1976) Effects of histamine and serotonin on isolated perfused gill of rainbow trout (Salmo gairdneri). Fed Proc 35:528 (1774)
Kisloff B, Moore EW (1976) Effect of serotonin on water and electrolyte transport in the in vivo rabbit small intestine. Gastroenterology 71:1033–1038
Klyce SD, Palkama KA, Harkonen M, Marshall WS, Huhtanii S, Mann KP, Neufeld AH (1982) Neural serotonin stimulates chloride transport in the rabbit corneal epithelium. Invest Ophthalmol Vis Sci 23:181–192
Koslow SH (1976) The biochemical and behavioral profile of 5- methoxytryptamine. In: Usdin E, Sandler M (eds) Trace amine and the brain. Dekker, New York, pp 103–130
Laurent P, Dunel S (1976) Functional organization of the teleost gill. I. Blood pathways. Acta Zool Stockholm 57:189–209
Laurent P, Dunel S (1980) Morphology of gill epithelia in fish. Am J Physiol 238:R147-R159
Nilsson S (1973) On the autonomic nervous control of organs in teleostean fishes. In: Bolis L, Schmidt-Nielsen K, Madrell SHP (eds) Comparative Physiology. North-Holland Publ., Amsterdam, pp 325–331
Nilsson S (1984) Innervation and pharmacology of the gills. In: Hoar WS, Randall DJ (eds) Fish Physiology. Academic Press, New York, pp 185–229
Nilsson S, Pettersson K (1981) Sympathetic nervous control of blood flow in the the gills of the Atlantic cod, Gadus morhua. J Comp Physiol 144:157–163
Östlund E, Fänge R (1962) Vasodilation by adrenaline and nordrenaline, and the effects of some other substances on perfused fish gills. Comp Biochem Physiol 5:307–309
Pasik P, Pasik T, Pecci Saavedra J (1982) Immunocytochemical localization of serotonin at ultrastructural level. J Histochem Cytochem 30:760–764
Patel S, Dulluc J, Geffard M (1986) Comparison of serotonin and 5-methoxytryptamine immunoreactivity in rat raphe nuclei. Histochem 85:259–263
Pettersson K (1983) Adrenergic control of oxygen transfer in perfused gills of the cod Gadus morhua. J Exp Biol 102:327–335
Pettersson K, Johansen K (1982) Hypoxic vasoconstriction and the effects of adrenaline on gas exchange efficiency in fish gills. J Exp Biol 97:263–272
Pettersson K, Nilsson S (1979) Nervous control of the branchial vascular resistance of the Atlantic cod, Gadus morhua. J Comp Physiol 129:179–183
Randall DJ, Stevens ED (1967) The role of adrenergic receptors in cardiovascular changes associated with exercise in salmon. Comp Biochem Physiol 21:415–424
Reinach PS, Candia OA (1978) Effects of tryptamine on active Na and chloride transport in the isolated bullfrog cornea. Biochim Biophys Acta 510:327–338
Reite OB (1969) The evolution of vascular smooth muscle responses to histamine and 5-hydroxytryptamine. Acta Physiol Scand 75:221–239
Santer RM, Holmgren S (1983) An ultrastructural and fluorescence histochemical study of the myenteric plexus of the stomach of the rainbow trout Salmo gairdneri. Acta Zool Stockholm 64:55–66
Scheide JI, Dietz TH (1983) Serotonin stimulated adenylate cyclase in the gill of a freshwater mussel and its relationship to sodium transport. Physiol Zool 56:585–596
Scheide JI, Dietz TH (1984) The effects of calcium on serotonin stimulated adenylate cyclase in freshwater mussels. Biol Bull (Woods Hole, Mass) 166:594–607
Smith DG (1977) Sites of cholinergic vasoconstriction in trout gills. Am J Physiol 233:R222-R229
Smith FM, Jones DR (1978) Localization of receptors causing hypoxic bradycardia in trout. Can J Zool 56:1260–1265
Sternberger LA (1979) Immunocytochemistry (2nd ed) In: Cohen S, McClusbey (eds) Basic and clinical immunology. Wiley J & Sons, New York
Tamir H, Gershon MD (1979) Storage of serotonin and serotonin binding protein in synaptic vesicles. J Neurochem 33:35–44
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Bailly, Y., Dunel-Erb, S., Geffard, M. et al. The vascular and epithelial serotonergic innervation of the actinopterygian gill filament with special reference to the trout, Salmo gairdneri . Cell Tissue Res. 258, 349–363 (1989). https://doi.org/10.1007/BF00239455
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00239455