Skip to main content
Log in

Mediation of serotonin-induced hyperventilation via 5-HT3-receptor in European eel Anguilla anguilla

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

The effects of serotonin (5-hydroxytryptamine) on ventilation were investigated by continuous measurements of intrabuccal pressure in unrestrained eel. Intravenous administration of 5-hydroxytryptamine (30 μg·kg-1) caused a large increase in ventilatory frequency (+100%) and amplitude (+140%). The 5-hydroxytryptamine-induced hyperventilation was blocked by the 5-HT3-receptor antagonists metoclopramide (1.0 mg·kg-1) or MDL72222 (1.0 mg·kg-1), and was insensitive to the 5-HT1/2-receptor antagonist methysergide (3.0 mg·kg-1) and to the 5-HT4-receptor antagonist DAU 6285 CL (3.0 mg·kg-1). The hyperventilatory response to 5-hydroxytryptamine could be mimicked by the 5-HT3 receptor agonist 1-phenylbiguanide (300 μg·kg-1). These results strongly implicate the 5-HT3-receptor as the mediator of the 5-hydroxytryptamine-induced hyperventilation in eel.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

a.u. :

arbitrary units

5-HT :

5-hydroxytryptamine

SEM :

standard error of mean

VA :

ventilatory amplitude

VF :

ventilatory frequency

RBI :

1-phenylbiguanide

References

  • Burleson ML, Milsom WK (1993) Sensory receptors in the first gill arch of rainbow trout. Respir Physiol 1:97–110

    Google Scholar 

  • Cameron JN, Wohlschlag DE (1969) Respiratory response to experimentally induced anaemia in the pinfish (Lagodon rhomboides). J Exp Biol 50:307–317

    Google Scholar 

  • Champagnat J, Denavit-Saubié M, Henry JL, Leviel V (1979) Catecholaminergic depressant effects on bulbar respiratory mechanisms. Brain Res 160:57–68

    Google Scholar 

  • Donald R, Mc Grimmon DR, Lalley PM (1982) Inhibition of respiratory neural discharges by clonidine and 5-hydroxytryptophan. J Pharmacol Exp 222:771–777

    Google Scholar 

  • Fallert M, Böhmer G, Dinse HRO, Sommer TJ, Bitner A (1979) Microelectrophoretic application of putative neurotransmitters onto various types of bulbar respiratory neurons. Arch Ital Biol 117:1–12

    Google Scholar 

  • Fritsche R, Thomas S, Perry SF (1992) Effects of serotonin on circulation and respiration in the rainbow trout, Oncorhynchus mykiss. J Exp Biol 173:59–74

    Google Scholar 

  • Gatti PJ, Dias Souza J, Namath IJ, Dasilva AMT, Holtman JR Jr, Gillis RA (1985) Comparative cardiorespiratory effects produced by taurine and glycine applied at the ventral surface of the medulla. J Pharmacol Exp Ther 235:280–282

    Google Scholar 

  • Genot G, Morfin R, Peyraud C (1981) Blood-brain barrier for serotonin in the eel, Anguilla anguilla L. Comp Biochem Physiol Vol 68C:247–250

    Google Scholar 

  • Gillis RA, Hill KJ, Kirby JS, Quest JA, Hamosh P, Norman WP, Kellar KJ (1989) Effects of activation of central nervous system serotonin 1A receptors on cardiorespiratory function. J Pharmacol Exp Ther 248:851–857

    Google Scholar 

  • Glowinski J, Axelrod J, Kopin IJ, Wurtam RJ (1964) Physiological disposition of 3H-norepinephrine in the developing rat. J Pharmacol 146:48–53

    Google Scholar 

  • Holeton GF (1971) Oxygen uptake and transport by the rainbow trout during exposure to carbon monoxide. J Exp Biol 54:239–254

    Google Scholar 

  • Holtman J Jr, Norman WP, Gillis RA (1984a) Projections from the raphe nuclei to the phrenic motor nucleus in the cat. Neurosci Lett 44:105–111

    Google Scholar 

  • Holtman JR Jr, Norman WP, Skirboll L, Dretchen KL, Cuello C, Visser TJ, Hokfelt T, Gillis RA (1984b) Evidence for 5-hydroxytryptamine, substance P and thyrotropin-releasing hormone in neurons innervating the phrenic motor nucleus. J Neurosci 4:1064–1071

    Google Scholar 

  • Hugues GM, Shelton G (1958) The mechanism of gill ventilation in three freshwater teleosts. J Exp Biol 35:807–823

    Google Scholar 

  • Labat R (1966) Electrocardiographie chez les poissons téléostéens: influence de quelques facteurs écologiques. Thèse de doctorat d'Etat. Toulouse

  • Lalley PB (1986) Serotonergic and non-serotonergic responses of phrenic motoneurones to raphe stimulation in the cat. J Physiol (London) 378:373–385

    Google Scholar 

  • Lindsay AD, Feldman JL (1993) Modulation of respiratory activity of neonatal rat phrenic motoneurones by serotonin. J Physiol (London) 461:213–233

    Google Scholar 

  • Liu G, Feldman JL, Smith JC (1990) Excitatory amino acid mediated transmission of inspiratory drive to phrenic motoneurons. J Neurophysiol 64:423–436

    Google Scholar 

  • Millhorn DE, Eldrige FL, Waldrop TG, Klinger LE (1983) Centrally and peripherally administered 5-HTP have opposite effects on respiration. Brain Res 264:349–354

    Google Scholar 

  • Milsom MK, Brill RW (1986) Oxygen-sensitive afferent information arising from the first gill arch of yellowfin tuna. Respir Physiol 66:193–203

    Google Scholar 

  • Monteau R, Morin D, Hennequin S, Hilaire G (1990) Differential effects of serotonin on respiratory activity of hypoglossal and cervical motoneurons: an in vitro study on the newborn rat. Neurosci Lett 111:127–132

    Google Scholar 

  • Morin D, Hennequin S, Montau R, Hilaire G (1990) Serotonergic influences on central respiratory activity: an in vitro study in the newborn rat. Brain Res 535:281–287

    Google Scholar 

  • Morin D, Monteau R, Hilaire G (1991) Serotonin and cervical respiratory motoneurones: intracellular study in the newborn rat brainstem-spinal cord preparation. Exp Brain Res 84:229–232

    Google Scholar 

  • Parent A, Poitras D, Dubé L (1984) Comparative anatomy of central monoaminergic systems. In: Björklund A, Hölkfelt T (eds) Handbook of chemical Neuroanatomy, vol 2. Classical transmitters in the CNS, Part I. Elsevier, Amsterdam, pp 409–439

    Google Scholar 

  • Peyraud-Waïtzenegger M, Savina A, Laparra J, Morfin R (1979) Blood-brain barrier for epinephrine in the eel (Anguilla anguilla L.). Comp Biochem Physiol 63C:35–38

    Google Scholar 

  • Peyraud-Waïtzenegger M, Barthelemy L, Peyraud C (1980) Cardiovascular and ventilatory effects of catecholamines in unrestrained eels (Anguilla anguilla L.). J Comp Physiol 138:367–375

    Google Scholar 

  • Rampin O, Pierrefiche O, Denavit-Saubié M (1993) Effects of serotonin and substance P on bulbar respiratory neurons in vivo. Brain Res 622:185–193

    Google Scholar 

  • Schmid K, Bohmer G, Merkelbach S (1990) Serotonergic control of phrenic motoneuronal activity at the level of the spinal cord of the rabbit. Neurosci Lett 116:204–209

    Google Scholar 

  • Sessle BL, Henry JL (1985) Effects of enkephalin and 5-hydroxytryptamine on solitary tract neurones involved in respiration and respiratory reflexes. Brain Res 327:221–230

    Google Scholar 

  • Smith FM, Jones DR (1982) The effect of changes in blood oxygen-carrying capacity on ventilation volume in the rainbow trout (Salmo gairdneri). J Exp Biol 97:325–334

    Google Scholar 

  • Suzue T (1984) Respiratory rhythm generation in the in vitro brainstem-spinal cord preparation of neonatal rat. J Physiol (London) 93:173–183

    Google Scholar 

  • Thomas S, Belaud A, Peyraud C (1979) Arguments for serotonergic adjustments in gill blood circulation in fish. IRCS Medical Science: Cardiovascular System; Environmental Biology and Medicine; Experimental Animals; Physiology; Respiratory System 7:743

    Google Scholar 

  • Wallen P, Buchanan JT, Grillner S, Hill RH, Christenson J, Hokfelt T (1989) Effects of 5-hydroxytryptamine on the after-hyperpolarization, spike frequency regulation and oscillatory membrane properties in lamprey spinal cord neurons. J Neurophysiol 61:759–768

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by H. Langer

Rights and permissions

Reprints and permissions

About this article

Cite this article

Janvier, J.J., Peyraud-Waïtzenegger, M. & Soulier, P. Mediation of serotonin-induced hyperventilation via 5-HT3-receptor in European eel Anguilla anguilla . J Comp Physiol B 165, 640–646 (1996). https://doi.org/10.1007/BF00301132

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00301132

Key words

Navigation