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Behavioral and cellular effects of serotonin on locomotion and male mating posture in Ascaris suum (Nematoda)

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Abstract

The site and mode of action of serotonin on locomotion were investigated in the parasitic nematode Ascaris suum. Injection of serotonin into Ascaris immediately caused paralysis in animals that were generating locomotory waveforms. Injected serotonin also increased body length and decreased the number of propagating body waves. Similar injections into the male tail produced a ventral tail curl. Injection of N-acetyl-serotonin had no effect on the generation of locomotory waveforms, but increased the body length and decreased the number of body waves in the waveform. Other biogenic amines were also tested but were much less potent.

Serotonin decreased the amplitude of a submaximal acetylcholine-induced muscle contraction and increased the time to attain this contraction. The time course of this effect on the response to ACh was much slower than the action of injected serotonin on locomotory waveforms, suggesting that additional elements are involved in the action of serotonin on locomotory behavior.

Serotonin abolished spontaneous slow potentials in VI motor neurons and decreased the frequency of EPSPs in DE2 motor neurons, probably by a pre-synaptic mechanism. In the male tail, serotonin depolarized the male-specific transverse ventral muscle cells, but did not affect either dorsal or ventral longitudinal muscle cells.

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Abbreviations

ACh :

acetylcholine

cAMP :

cyclic adenosine monophosphate

DA :

dopamine

DE :

dorsal excitatory motor neuron

DI :

dorsal inhibitory motor neuron

DM :

dorsal muscle

ELP :

egg-laying pore

EPSP :

excitatory post synaptic potential

GABA :

gamma aminobutyric acid

HRB :

head restricted behavior

IPSP :

inhibitory post synaptic potential

5-HT :

5-hydroxytryptamine, serotonin

NA-5-HT :

N-acetyl-5-hydroxytryptamine

NE :

norepinephrine

OA :

octopamine

PBS :

phosphate buffered saline

PCF :

pseudocoelomic fluid

tVM :

malespecific transverse ventral muscle

TRYP :

tryptamine

VI :

ventral inhibitory motor neuron

References

  • Albertson D, Thomson N (1976) The pharynx of Caenorhabditis elegans. Phils Trans R Soc Lond B 275: 299–325

    Google Scholar 

  • Angstadt JD (1986) Ph.D. Thesis, University of Wisconsin, Madison, Wisconsin

    Google Scholar 

  • Ash ASF, Tucker JF (1967) The bioassay of γ-aminobutyric acid using a muscle preparation from Ascaris lumbricoides. J Pharm Pharmacol 19: 240–245

    Google Scholar 

  • Baldwin E, Moyle V (1947) An isolated nerve-muscle preparation from Ascaris lumbricoides. J Exp Biol 23: 277–291

    Google Scholar 

  • Brownlee DJA, Fairweather I, Johnston CF (1994) Immunocytochemical demonstration of peptidergic and serotoninergic components in the enteric nervous system of the round worm Ascaris suum (Nematoda, Ascaroidea). Parasitology 108: 89–103

    Google Scholar 

  • Chaudhuri J, Donahue MJ (1989) Serotonin receptors in the tissues of adult Ascaris suum. Mol Biochem Parasitol 35: 191–198

    Google Scholar 

  • Cowden C, Stretton AOW (1993) AF2, an Ascaris neuropeptide: isolation, sequence, and bioactivity. Peptides 14: 423–430

    Google Scholar 

  • Cowden C, Stretton AOW (1995) Eight novel FMRFamide-like neuropeptides isolated from the nematode Ascaris suum. Peptides 16: 491–500

    Google Scholar 

  • Cowden C, Stretton AOW, Davis RE (1989) AF1, a sequenced bioactive neuropeptide isolated from the nematode Ascaris suum. Neuron 2: 1465–1473

    Google Scholar 

  • Cowden C, Sithigorngul P, Brackley J, Guastella J, Stretton AOW (1993) Localization and differential expression of FMRFamidelike immunoreactivity in the nematode Ascaris suum. J Comp Neurol 333: 455–468

    Google Scholar 

  • Davis RE, Stretton AOW (1989) Passive membrane properties of motor neurons and their role in long-distance signaling in the nematode Ascaris. J Neurosci 9: 403–414

    Google Scholar 

  • del Castillo J, de Mello WE, Morales T (1963) The physiological role of acetylcholine in the neuromuscular system of Ascaris lumbricoides. Arch Internat Physiol Biochim 71: 741–757

    Google Scholar 

  • del Castillo J, de Mello WE, Morales T (1964) Inhibitory action of γ-aminobutyric acid (GABA) on Ascaris muscle. Experientia 20: 141–143

    Google Scholar 

  • Guastella J, Johnson CD, Stetton AOW (1991) GABA-Immunoreactive neurons in the nematode Ascaris. J Comp Neurol 307: 584–597

    Google Scholar 

  • Harris-Warrick RM, Marder E (1991) Modulation of neural networks for behavior. Ann Rev Neurosci 14: 39–57

    Google Scholar 

  • Horvitz HR, Chalfie M, Trent C, Sulston JE, Evans PD (1982) Serotonin and octopamine in the nematode Caenorhabditis elegans. Science 216: 1012–1014

    Google Scholar 

  • Isaac RE, Eaves L, Lamango N (1991) N-acetylation of biogenic amines in Ascaridia galli. Parasitology 102: 445–450

    Google Scholar 

  • Johnson CD, Stretton AOW (1985) Localization of choline acetyltransferase within identified motor neurons of the nematode Ascaris. J Neurosci 5: 1984–1992

    Google Scholar 

  • Johnson CD, Stretton AOW (1987) GABA-immunoreacitivty in inhibitory neurons of the nematode Ascaris. J Neurosci 7: 223–235

    Google Scholar 

  • Johnson CD, Reinitz CA, Sithigorngul P, Stretton AOW (1996) Neuronal localization of serotonin in the nematode Ascaris suum. J Comp Neurol (in press)

  • C. A. Reinitz, A. O. W. Stretton: Effects of serotonin in Ascaris

  • Kass IS, Larsen DA, Wang CC, Stretton AOW (1982) Ascaris suum: Differential effects of avermectin B1a on the intact animal and neuromuscular strip preparations. Exp Parasitol 54: 166–174

    Google Scholar 

  • Kass IS, Stretton AOW, Wang CC (1984) The effects of avermectin and drugs related to acetylcholine and γ-aminobutyric acid on neurotransmission in Ascaris suum. Mol Biochem Parasitol 13: 213–225

    Google Scholar 

  • Loer CM, Kenyon CJ (1993) Serotonin-deficient mutants and male mating behavior in the nematode Caenorhabditis elegans. J Neurosci 13: 5407–5417

    Google Scholar 

  • Mansour T (1984) Serotonin receptors in parasitic worms. Adv Parasitol 23: 1–36

    Google Scholar 

  • Martin RJ (1985) Gamma-aminobutyric acid- and piperazine-activated single channel currents from Ascaris suum body muscle. Br J Pharm 84: 445–461

    Google Scholar 

  • McIntire SL, Jorgensen E, Horvitz HR (1993a) Genes required for GABA function in Caenorhabditis elegans. Nature 364: 334–337

    Google Scholar 

  • Mclntire SL, Jorgensen E, Kaplan J, Horvitz HR (1993b) The GABAergic nervous system of Caenorhabditis elegans. Nature 364: 337–341

    Google Scholar 

  • Meade JA, Stretton AOW (1987) Intracellular recordings during locomotion of intact Ascaris lumbricoides. Soc Neurosci Abstr 13: 1060

    Google Scholar 

  • Russell RL, Rand JB (1986) Structural gene mutations affecting acetylcholinesterase and choline acetyltransferase perturb behavior in a simple invertebrate. In: Hanin I (ed) Dynamics of cholinergic function. Plenum Press, New York, pp 799–816

    Google Scholar 

  • Segerberg MA, Stretton AOW (1993) Actions of cholinergic drugs in the nematode Ascaris suum. J Gen Physiol 101: 271–296

    Google Scholar 

  • Stretton AOW, Johnson CD (1985) GABA and 5-HT immunoreactive neurons in Ascaris. Soc Neurosci Abstr 11: 626

    Google Scholar 

  • Stretton AOW, Fishpool RM, Southgate E, Donmoyer JE, Walrond JP, Moses JER, Kass IS (1978) Structure and physiological activity of the motoneurons of the nematode Ascaris. Proc Natl Acad Sci USA 75: 3493–3497

    Google Scholar 

  • Walrond JP, Kass IS, Stretton AOW, Donmoyer JE (1985) Identification of excitatory and inhibitory motoneurons in the nematode Ascaris by electrophysiological techniques. J Neurosci 5: 1–8

    Google Scholar 

  • Ward S, Thomson N, White J, Brenner S (1975) Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. J Comp Neurol 160: 313–338

    Google Scholar 

  • White JG, Southgate E, Thomson JN, Brenner S (1976) The structure of the ventral nerve cord of Caenorhabditis elegans. Phil Trans R Soc Lond B 275: 327–348

    Google Scholar 

  • White JG, Southgate E, Thomson JN, Brenner S (1986) The structure of the nervous system of Caenorhabditis elegans. Phil Trans R Soc Lond B 314: 1–340

    Google Scholar 

  • Williams JA, Shahkolahi AM, Abbassi M, Donahue MJ (1992) Identification of a novel 5-HTN (Nematoda) receptor from Ascaris suum muscle. Comp Biochem Physiol 101 C: 469–474

    Google Scholar 

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Author notes

  1. C. A. Reinitz

    Present address: Department of Biochemistry and Molecular Biology, University of North Dakota School of Medicine, 58202, Grand Forks, ND, USA

Authors and Affiliations

  1. Neuroscience Training Program and Department of Zoology, University of Wisconsin, 53706, Madison, Madison, WI, USA

    C. A. Reinitz & A. O. W. Stretton

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  1. C. A. Reinitz
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  2. A. O. W. Stretton
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Reinitz, C.A., Stretton, A.O.W. Behavioral and cellular effects of serotonin on locomotion and male mating posture in Ascaris suum (Nematoda). J Comp Physiol A 178, 655–667 (1996). https://doi.org/10.1007/BF00227378

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