Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-23T02:25:50.048Z Has data issue: false hasContentIssue false
  • English
  • Français

The motornervous system of Ascaris: electrophysiology and anatomy of the neurons and their control by neuromodulators

Published online by Cambridge University Press:  06 April 2009

R. E. Davis  and
A. O. W. Stretton
R. E. Davis
Affiliation:
Department of Zoology, University of Wisconsin-Madison, Madison, WI 53706, USA
A. O. W. Stretton*
Affiliation:
Department of Zoology, University of Wisconsin-Madison, Madison, WI 53706, USA
*
*Corresponding author.
Get access Rights & Permissions [Opens in a new window]

Summary

Analysis of the electrical properties of neurons in the motornervous system of Ascaris suum suggests that it is largely an analogue system. The motorneurons do not conduct action potentials and they release transmitter tonically at their normal resting potential; transmitter release is increased or decreased as a continuous function of membrane potential. Despite extensive physiological descriptions of the electrical properties of the neurons and their synapses, as well as morphological descriptions of the synaptic circuitry of the system, the predicted activities of the neurons in the circuit differ from those observed by direct recording in semi-intact behaving animals. We conclude that the description of the circuit is incomplete. There are several possibilities for the missing elements, including chemical, proprioceptive, and additional neuronal components. Recently, attention has been focussed most heavily on the intercellular chemical signalling systems; in addition to those mediated by classical neurotransmitters, a surprisingly complex array of neuropeptides has been identified. One family of these peptides, the AF peptides, has been analyzed in detail. It comprises at least 20 peptides, and they fall into sequence-related subfamilies. One of these subfamilies, containing 6 peptides, is encoded by a single transcript, suggesting that the AF peptides are under multiple genetic control. All AF peptides tested have potent activity on the motornervous system and or on muscle. There are multiple physiological activities, and cellular localization studies show multiple patterns of cellular expression. Studies on Panagrellus and Caenorhabditis emphasize the diversity of this family and its genetic control.

Keywords

Ascarisnematodemotornervous systemneuromodulatorsneuropeptides
Type
Research Article
Information
Parasitology , Volume 113 , supplement S1: Molecular biochemistry and physiology of helminth neuromuscular systems , January 1996 , pp. S97 - S117
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Adams, M. E. & O'Shea, M. (1983). Peptide cotransmitter at a neuromuscular junction. Science 221, 286–9.Google Scholar
Angstadt, J. D. (1986). Anatomy and physiology of oscillatory neurons in the nematode Ascaris. Ph.D. Thesis. University of Wisconsin, Madison.Google Scholar
Angstadt, J. D., Donmoyer, J. E. & Stretton, A. O. W. (1989).Retrovesicular ganglion of the nematode Ascaris. Journal of Comparative Neurology 284, 374–88.CrossRefGoogle ScholarPubMed
Angstadt, J. D. & Stretton, A. O. W. (1989). Slow active potentials in ventral inhibitory motor neurons of the nematode Ascaris. Journal of Comparative Physiology A 166, 165–77.Google ScholarPubMed
Balcar, v. J. & Johnston, G. A. R. (1972a). Glutamate uptake by brain slices and its relation to the depolarization of neurones by acidic amino acids. Journal of Neurobiology 3, 295–301.CrossRefGoogle Scholar
Balcar, V. J. & Johnston, G. A. R. (1972b). The structural specificity of the high affinity uptake of L-glutamate and L-aspartate by rat brain slices. Journal of Neurochemistry 19, 2657–66.Google Scholar
Bascal, Z., Holden-DYE, L., Willis, R. J., Smith, S. W. G. & Walker, R. j. (1996). Novel azole deriviatives are antagonists at the inhibitory GABA receptor on the somatic muscle cells of the parasitic nematode Ascaris suum. Parasitology 112, 253–9.Google Scholar
Blight, A. R. & Llinas, R. (1980). The non-impulsive stretch receptor complex of the crab; a study of depolarization-release coupling at a tonic sensorimotor synapse. Philosophical Transactions of the Royal Society of London [Biology] 290, 219–76.Google Scholar
Bowman, J. W., Geary, T. G. & Thompson, D. P. (1990). Electrophysiological characterization of the effects of nematode FMRFamide-like neuropeptides on Ascaris suum muscles. Abstracts, Neurotox 90, 129.Google Scholar
Bowman, J. W., Winterrowd, C. A., Friedman, A. R., Thompson, D. P., Klein, R. D., Davis, J. P., Maule, A.G., Blair, K. L. & Geary, T. G. (1995). Nitric oxide mediates the inhibitory effects of SDPNFLRFamide, a nematode FMRFamide-related peptide, in Ascaris suum. Journal of Neurophysiology 74, 1880–8.CrossRefGoogle ScholarPubMed
Brading, A. F. & Caldwell, p.c. (1971). The resting membrane potential of the somatic muscle cells of Ascaris lumbricoides. Journal of Physiology 217, 605–24.CrossRefGoogle ScholarPubMed
Brew, H. & Attwell, D. (1987). Electrogenic glutamate uptake is a major current carrier in the membrane of axolotl retinal glial cells. Nature 327, 707–9.Google Scholar
Brownlee, D. J. A., Fairweather, I. & Johnston, C. F. (1993a). Immunocytochemical demonstration of neuropeptides in the peripheral nervous system of the roundworm Ascaris swum (Nematoda, Ascaroidea). Parasitology Research 79, 302–8.Google Scholar
Brownlee, D. J. A., Fairweather, I., Johnston, C. F. & Shaw, c. (1994). Immunocytochemical demonstration of peptidergic and serotoninergic components of the enteric nervous system of the roundworm, Ascaris suum (Nematoda, Ascaroidea). Parasitology 108, 89–103.Google Scholar
Brownlee, D. J. A., Fairweather, I., Johnston, C. F., Smart, D., Shaw, C. & Halton, D. W. (1993 b). Immunocytochemical demonstration of neuropeptides in the central nervous system of the roundworm, Ascaris suum (Nematoda: Ascaroidea). Parasitology 106, 305–16.CrossRefGoogle ScholarPubMed
Bush, B. M. H. (1976). Non-impulsive thoracic coxal receptors in crustaceans. In Structure and Function of Proprioceptors in the Invertebrates (ed. Mill, P. J.), pp. 115–51. London: Chapman and Hall.Google Scholar
Byerly, L. & Masuda, M. o. (1979). Voltage-clamp analysis of the potassium current that produces a negative-going action potential in Ascaris muscle. Journal of Physiology (London) 288, 263–84.Google Scholar
Cannone, A. J. & Bush, B. M. H. (1980). Reflexes mediated by non-impulsive afferent neurones of thoracic-coxal muscle receptor organs in the crab, Carcinus maenas. 2. Reflex discharge evoked by current injections. Journal of Experimental Biology 86, 305–31.Google Scholar
Colquhoun, L., Holden-DYE, L. & Walker, R. J. (1991). The pharmacology of cholinoceptors on the somatic muscle cells of the parasitic nematode Ascaris suum. Journal of Experimental Biology 158, 509–30.CrossRefGoogle ScholarPubMed
Cowden, C, Sithigorngul, P., Brackley, P., Guastella, J. & Stretton, A. o. w. (1993). Localization and differential expression of FMRFamide-like immunoreactivity in the nematode Ascaris suum. Journal of Comparative Neurology 333, 455–68.CrossRefGoogle ScholarPubMed
Cowden, c. & Stretton, A. o. w. (1993). AF2, an Ascaris neuropeptide: isolation, sequence and bioactivity. Peptides 14, 423–30.Google ScholarPubMed
Cowden, c. & Stretton, A. o. w. (1995). Eight novel FMRFamide-like neuropeptides isolated from the nematode Ascaris suum. Peptides 16, 491–500.CrossRefGoogle ScholarPubMed
Cowden, C, Stretton, A. O. W. & Davis, R. E. (1989). AF1, a sequenced bioactive neuropeptide isolated from the nematode Ascaris. Neuron 2, 1465–73.Google Scholar
Crofton, H. D. (1966). Nematodes. London: Hutchinson University Library.Google Scholar
Cully, D. F., Vassilitis, D. K., Liu, K. K., Paress, P. S., Vanderploeg, L. H. T. & Schaeffer, J. M. (1994).Cloning of an avermectin-sensitive glutamate-gated chloride channel from Caenorhabditis elegans. Nature 371, 707–11.CrossRefGoogle Scholar
Davenport, T. R. B., Lee, D. L. & Isaac, R. E. (1988). Immunocytochemical demonstration of a neuropeptide in Ascaris suum (Nematoda) using an antiserum to FMRFamide. Parasitology 97, 81–8.Google Scholar
Davis, R. E. (1984). Membrane properties and synaptic interactions of motorneurons in the nematode Ascaris. Ph.D. Thesis. University of Wisconsin - Madison.Google Scholar
Davis, R. E. (1996a). Action of excitatory amino acids in the motornervous system of the nematode Ascaris suum. I. Pharmacological evidence for a kainate receptor. Journal of Neurophysiology (in press).Google Scholar
Davis, R. E. (1996b). Action of excitatory amino acids in the motornervous system of the nematode Ascaris suum. II. Pharmacological evidience for a glutamate transporter. Journal of Neurophysiology (in press).Google Scholar
Davis, R. E. & Stretton, A. O. W. (1989a). Passive membrane properties of motorneurons and their role in long distance signaling in the nematode Ascaris. Journal of Neuroscience 9, 403–14.CrossRefGoogle ScholarPubMed
DAVIS, R. E. & Stretton, A. O. w. (19896). Signaling properties of Ascari motorneurons: graded active responses, graded synaptic transmission, and tonic transmitter release. Journal of Neuroscience 9, 415–25.Google Scholar
Davis, R. E. & Stretton, A. O. W. (1992). Extracellular recordings from the motor nervous system of the nematode, Ascaris suum. Journal of Comparative Physiology A 171, 17–28.Google ScholarPubMed
Davis, R. E. & Stretton, A. O. W. (1995). Neurotransmitters of helminths. In Biochemistry and Molecular Biology of Parasites (ed. Marr, J. J. & Muller, M.), pp. 257–87. New York, Academic Press.Google Scholar
De Bell, J. T., Del Castillo, J. & Sanchez, V. (1963). Electrophysiology of the muscle cells of Ascaris lumbricoides. Journal of Cellular and Comparative Physiology 62, 159–78.Google Scholar
Del Castillo, J., De Mello, W. C. & Morales, T. (1963). The physiological role of acetylcholine in the neuromuscular system of Ascaris lumbricoides. Archives d'Internationale Physiologie et Biochimie 71, 741–57.CrossRefGoogle Scholar
Del Castillo, J., De Mello, W. C. & Morales, T. (1964a). Inhibitory action of gamma aminobutyric acid (GABA) on Ascaris muscle. Experientia 20, 141–3.Google Scholar
Del Castillo, J., De Mello, W. C. & Morales, T. (1964b). Mechanism of the paralysing action of piperazine on Ascaris muscle. British Journal of Pharmacology 22, 463–77.Google Scholar
Del Castillo, J., De MELLO, W. C. & Morales, T. (1967). The initiation of action potentials in the somatic muscle of Ascaris lumbricoides. Journal of Experimental Biology 46, 263–79.CrossRefGoogle ScholarPubMed
Detwiler, P. B., Hodgkin, A. L. & Mcnaughton, P. A. (1978). A surprising property of electrical spread in the network of rods in the turtle's retina. Nature 274, 562–5.Google Scholar
Duittoz, A. H. & Martin, R. J. (1991). Effects of the arylaminopyrazine-GABA derivatives SR95103 and SR 95531 on the Ascaris muscle GABA receptor: the relative potency of the antagonists in Ascaris is different to that at vertebrate GABAa receptors. Comparative Biochemistry and Physiology 98C, 417–22.Google Scholar
Eliasof, S. & Werblin, F. (1993). Characterization of the glutamate transporter in retinal cones of the tiger salamander. Journal of Neuroscience 13, 402–11.CrossRefGoogle ScholarPubMed
Franks, C. J., Holden-DYE, L., Williams, R. G., Pang, F.Y. & Walker, R. J. (1994). A nematode FMRFamide-like peptide, SDPNFLRF amide (PF1), relaxes the dorsal muscle strip preparation of Ascaris suum. Parasitology 108, 229–36.Google Scholar
Geary, T. G., Price, D. A., Bowman, J. W., Winterrowd, C. A., Mackenzie, C. D., Garrison, R. D., Williams, J. F. & Friedman, A. R. (1992). Two FMRFamide-like peptides from the free-living nematode Panagrellus redivivus. Peptides 13, 209–14.Google Scholar
Goldschmidt, R. (1908). Das nervensystem von Ascaris lumbricoides und megalocmephala. Ein Versuch in den Aufbau eines einfacken Nervensystem einzudringen. Zeitschrift fur Wissenschaftliche Zoologie 90, 73–136.Google Scholar
Goldschmidt, R. (1909). Das nervensystem von Ascaris lumbricoides und megalocephala. Ein Versuch in den Aufbau eines einfacken Nervensystem einzudringen. II. Zeitschrift fiir Wissenschaftliche Zoologie 92, 306–57.Google Scholar
Goldschmidt, R. (1910). Das nervensystem von Ascaris lumbricoides und megalocephala. Ein Versuch in den Aufbau eines einfacken Nervensystem einzudringen. III. Festschrift fur R. Hertzvig, Jena 2, 256–354.Google Scholar
Graubard, K. (1978). Synaptic transmission without action potentials: input-ouput properties of a non-spiking presynaptic neuron. Journal of Neurophysiology 41, 1014–25.CrossRefGoogle Scholar
Guastella, J. & Stretton, A. o. w. (1991). Distribution of 3H-GABA uptake sites in the nematode Ascaris. Journal of Comparative Neurology 307, 598–608.Google Scholar
Guastella, J., Johnson, C. D. & Stretton, A. O. W. (1991). GABA-immunoreactive neurons in the nematode Ascaris. Journal of Comparative Neurology 307, 584–97.Google Scholar
Harris, J. E. & Crofton, H. D. (1957). Structure and function in the nematodes: internal pressure and cuticular structure in Ascaris. Journal of Experimental Biology 34, 116–30.CrossRefGoogle Scholar
Hodgkin, A. L. & Rushton, w. A. H. (1946). The electrical constants of a crustacean nerve fibre. Proceedings of the Royal Society of London [Biology] 133, 444–79.Google Scholar
Holden-DYE, L., Krogsgaard-LARSEN, P., Neilsen, L. & Walker, R. J. (1989). GABA receptors on the somatic muscle cells of the parasitic nematode, Ascaris suum: stereoselectivity indicates similarity to a GABAa-type agonist recognition site. British Journal of Pharmacology 98, 841–51.CrossRefGoogle ScholarPubMed
Holden-DYE, L. & Walker, R. J. (1994). Characterization of identifiable neurones in the head ganglia of the parasitic nematode Ascaris suum: a comparison with central neurones of Caenorhabditis elegans. Parasitology 108, 81–7.Google Scholar
Horvitz, R. H., Chalfie, M., Trent, C, Sulston, J. E. & Evans, P. D. (1982). Serotonin and octopamine in the nematode Caenorhabditis elegans. Science 206, 1012–14.Google Scholar
Hudspeth, A. J., Poo, M. M. & Stuart, A. E. (1977). Passive signal propagation and membrane properties in median photoreceptors of the giant barnacle. Journal of Physiology (London) 272, 25–43.Google Scholar
Isaac, R. E., Eaves, L., Muimo, R. & Lamango, M. (1991). N-acetylation of biogenic amines in Ascaridia galli. Parasitology 102, 445–50.CrossRefGoogle ScholarPubMed
Jarman, M. (1959). Electrical activity in the muscle cells of Ascaris lumbricoides. Nature 184, 1244.CrossRefGoogle Scholar
Johnson, C. D., Reinitz, C. A., Sithigorngul, P. & Stretton, A. o. w. (1996). Neuronal localization of S115 serotonin in the nematode Ascaris suum. Journal of Comparative Neurology 367, 352–60.Google Scholar
Johnson, c. D. & Stretton, A. o. w. (1985). Localization of choline acetyltransferase within identified motorneurons of the nematode Ascaris. Journal of Neuroscience 5, 1984–992.Google Scholar
Johnson, C. D. & Stretton, A. O. W. (1987). GABA-immunoreactivity in inhibitory motor neurons of the nematode Ascaris. Journal of Neuroscience 7, 223–35.Google Scholar
Kass, I. S., Stretton, A. O. W. & Wang, C. C. (1984). The effects of avermectin and drugs related to acetylcholine and 4-aminobutryric acid on neurotransmission in Ascaris suum. Molecular and Biochemical Parasitology 13, 213–25.Google Scholar
Loer, c. M. & Kenyon, c. J. (1993). Serotonin-deficient mutants and male mating behavior in the nematode Caenorhabditis elegans. Journal of Neuroscience 13, 5407–17.CrossRefGoogle ScholarPubMed
Lowe, D. A., Bush, B. M. H. & Ripley, S. H. (1978). Pharmacological evidence for ‘fast’ sodium channels in non-spiking neurons. Nature 274, 289–90.CrossRefGoogle Scholar
Mansour, T. E. (1984). Serotonin receptors in parasitic worms. Advances in Parasitology 23, 1–36.Google ScholarPubMed
Marder, E., Calabrese, R. L., Nusbaum, M. P. & Trimmer, B. (1987). Distribution and partial characterization of FMRFamide-like peptides in the stomatogastric nervous system of the rock crab, Cancer borealis, and the spiny lobster, Panulirus interruptus. Journal of Comparative Neurology 259, 150–63.Google Scholar
Marks, N. J., Shaw, C. J., Maule, A. G., Davis, J. P., Halton, D. W., Verrhaert, P., Geary, T. G. & Thompson, D. P. (1995). Isolation of AF2 (KHEYLRFamide) from Caenorhabditis elegans: evidence for the presence of more than one FMRFamide-related peptide-encoding gene. Biochemical and Biophysical Research Communications 217, 845–51.CrossRefGoogle ScholarPubMed
Martin, R. J. (1982). Electrophysiological effects of piperazine and diethylcarbazine on Ascaris suum somatic muscle. British Journal of Pharmacology 77, 255–65.Google Scholar
Martin, R. J. (1985). Gamma-aminobutyric acid-and piperazine-activated single channel currents from Ascaris suum body muscle. British Journal of Pharmacology 84, 445–61.Google Scholar
Martin, R. J. (1996). An electrophysiological preparation of Ascaris suum pharyngeal muscle reveals a glutamate-gated chloride channel sensitive to the avermectin analogue, milbemycin D. Parasitology 112, 247–52.Google Scholar
Martin, R. J., Pennington, A. J., Duittoz, A. H., Robertson, s. & Kusel, J. R. (1991). The physiology and pharmacology of neuromuscular transmission in the nematode parasite Ascaris suum. Parasitology 102, S41–S58.Google Scholar
Martin, R. J., Sitamze, J. M., Duittoz, A. H. & Wermuth, c. G. (1995). Novel arylaminopyridazine-GABA receptor antagonists examined electrophysiologically in Ascaris suum. European Journal of Pharmacology 276, 9–19.CrossRefGoogle ScholarPubMed
Maule, A. G., Shaw, C, Bowman, J. W., Halton, D. W., Thompson, D. P., Geary, T. G. & Thim, L. (1994). KSAYMRFamide: a novel FMRFamide-related heptapeptide from the free-living nematode, Panagrellus redivivus, which is myoactive in the parasitic nematode, Ascaris suum. Biochemical and Biophysical Research Communications 200, 973–80.CrossRefGoogle ScholarPubMed
Maule, A. G., Shaw, C, Bowman, J. W., Halton, D. W., Thompson, D. P., Thim, L., Kubiak, T. M., Martin, R. A. & Geary, T. G. (1995). Isolation and preliminary biological characterization of KPNFIRFamide, a novel FMRFamide-related peptide from the free-living nematode Panagrellus redivivus. Peptides 16, 87–93.Google Scholar
Mcgeer, p. L. & Mc-GEER, E.G. (1982) Kainic acid: the neurotoxic breakthrough. CRC Critical Reviews in Toxicology 10, 1–26.Google Scholar
McGEER, E. G., OLNEY, J. W. And McGEER, P., EDS. (1978). Kainic Acid as a Tool in Neurobiology. New York: Raven Press.Google Scholar
Meade, J. A. (1991). Intracellular recordings from neurons and muscle cells in a semi-intact preparation of the nematode Ascaris suum: implications for Ascaris locomotion. Ph.D. Thesis. University of Wisconsin-Madison.Google Scholar
Meade, J. A. & Stretton, A. o. w. (1989). Activity of motorneurons during Ascaris locomotion. Society for Neuroscience Abstracts 15, 1299.Google Scholar
Natoff, J. L. (1969). The pharmacology of the cholinoceptor in muscle preparations of Ascaris lumbricoides. British Journal of Pharmacology 37, 251–57.CrossRefGoogle ScholarPubMed
Parri, H. R., Holden-DYE, L. & Walker, R. J. (1991). Studies on the ionic selectivity of the GABA-operated chloride channel on the somatic muscle bag cells of the parasitic nematode Ascaris suum. Experimental Physiology 76, 597–606.CrossRefGoogle ScholarPubMed
Rall, w. (1977). Core conductor theory and cable properties of neurons. In Handbook of Physiology, Vol.1, Section 1, (ed., Kandel, E. R.), pp. 39–97. Bethesda MD: American Physiological SocietyGoogle Scholar
Reinitz, C. A. (1993). The role of serotonin in Ascaris suum locomotion. Ph.D. Thesis. University of Wisconsin - Madison.Google Scholar
Reinitz, c. A. & Stretton, A. O. W. (1996). Behavioral and cellular effects of serotonin on locomotion and male mating posture in Ascaris suum (Nematoda). Journal of Comparative Physiology A 178, 655–67.Google Scholar
Rohrer, S. P., Evans, W. D. & Bergstrom, A. (1990). A membrane associated glutamate binding protein from Caenorhabditis elegans and Haemonchus contortus. Comparative Biochemistry and Physiology 95C, 223–8.Google ScholarPubMed
Rosenbluth, J. (1965a). Ultrastructural organization of obliquely striated muscle fibres in Ascaris lumbricoides. Journal of Cell Biology 25, 495–515.CrossRefGoogle ScholarPubMed
Rosenbluth, J. (19656). Ultrastructure of somatic muscle cells in Ascaris lumbricoides II. Intermuscular junctions and glycogen stores. Journal of Cell Biology 26, 579–91.Google Scholar
Rosenbluth, J. (1967). Obliquely striated muscle III. Contraction mechanism of Ascaris body wall muscle. Journal of Cell Biology 34, 15–33.Google Scholar
Rosenbluth, J. (1969). Ultrastructure of dyads in muscle fibres of Ascaris lumbricoides. Journal of Cell Biology 42, 817–25.Google Scholar
Rosoff, M. L., Burglin, T. R. & Li, C. (1992). Alternatively spliced transcripts of the flp-1 gene encode distinct FMRFamide-like peptides in Caenorhabditis elegans. Journal of Neuroscience 12, 2356–61.Google Scholar
Rosoff, M. L., Doble, K. E., Price, D. A. & Li, C. (1993). The flp-1 gene propeptide is processed into multiple, highly similar FMRFamide-like peptides in Caenorhabditis elegans. Peptides 14, 331–8.CrossRefGoogle ScholarPubMed
Rozhkova, E. K., Malyutina, T. A. & Shishov, B. A. (1980). Pharmacological characteristics of cholinoception in the somatic muscles of the nematode Ascaris suum. General Pharmacology 11, 141–6.CrossRefGoogle Scholar
Schaeffer, J. M., White, T., Bergstrom, A. R., Wilson, K. E. & Turner, M. (1990). Identification of glutamate-binding sites in Caenorhabditis elegans. Pesticide Biochemisty and Physiology 36, 220–8.Google Scholar
Schneider, L. E. & Taghert, p. H. (1988). Isolation and characterization of a Drosophila gene encoding multiple neuropeptides related to FMRFamide (Phe-Met-Arg-Phe-NH2). Proceedings of the National Academy of Sciences, USA 85, 1993–7.Google Scholar
Schultz, J. E. & Schade, u. (1989). Veratridine induces a Ca2+ influx, cyclic GMP formation, and backward swimming in Paramecium tetraurelia wildtype cells and Ca2+ current-deficient pawn mutant cells. Journal of Membrane Biology 109, 251–8.Google Scholar
Segerberg, M. A. (1989). Nematode cholinergic pharmacology. Ph.D. Thesis. University of Wisconsin, Madison.Google Scholar
Segerberg, M. A. & Stretton, A. O. W. (1993). Actions of cholinergic drugs in the nematode Ascaris suum: complex pharmacology of muscle and motorneurons. Journal of General Physiology 101, 1–26.Google Scholar
Sithigorngul, P., Cowden, C, Guastella, J. & Stretton, A. o. w. (1989). Generation of monoclonal antibodies against nematode peptide extract: another approach for identifying unknown peptides. Journal of Comparative Neurology 284, 389–97.Google Scholar
Sithigorngul, P. & Stretton, A. O. W. (1991). Differential distribution of AF1, a FMRFamide-like peptide in the Ascaris nervous system, revealed by a specific monoclonal antibody. Abstracts of the Society for Neuroscience 17, 279.Google Scholar
Sithigorngul, P., Stretton, A. O. W. & Cowden, C. (1990). Neuropeptide diversity in Ascaris: an immunocytochemical study. Journal of Comparative Neurology 294, 362–76.Google Scholar
Sithigorngul, P., Cowden, C. & Stretton, A. O. W. (1996). Heterogeneity of cholecystokinin gastrin immunoreactivity in the nervous system of the nematode Ascaris suum. Journal of Comparative Neurology, 370: 427–42.Google Scholar
Stretton, A. o. w. (1992). Signalling systems in the nervous system of the nematode Ascaris. Neurotox 91 (ed., Duce, I. R.), pp. 124–138. Elsevier.Google Scholar
Stretton, A. O. W., Cowden, C, Sithigorngul, P. & Davis, R. E. (1991). Neuropeptides in the nematode Ascaris suum. Parasitology 102, S107–S116.Google Scholar
Stretton, A. O. W., Davis, R. E., Angstadt, J. D., Donmoyer, J. E. & Johnson, c. D. (1985). Neural control of behaviour in Ascaris. Trends in Neuroscience 8, 294–300.Google Scholar
Stretton, A. O. W., Donmoyer, J. E., Davis, R. E., Meade, J. A., Cowden, c. & Sithigorngul, p. (1992). Motor behavior and motor nervous system function in the nematode Ascaris suum. Journal of Parasitology 78, 206–14.CrossRefGoogle ScholarPubMed
Stretton, A. O. W., Fishpool, R. M., Southgate, E., Donmoyer, J. E., Walrond, J. P., Moses, J. E. R. & Kass, I. s. (1978). Structure and physiological activity of the motorneurons of the nematode Ascaris. Proceedings of the National Academy of Sciences, USA 75, 3493–7.Google Scholar
Stretton, A. O. W. & Johnson, C. D. (1985). GABA and 5HT immunoreactive neurons in Ascaris. Society for Neuroscience Abstracts 11, 626.Google Scholar
Tachibana, M. & Kaneko, A. (1988). L-glutamate-induced depolarization in solitary photoreceptors: a process that may contribute to the interaction between photoreceptors in situ. Proceedings of the National Academy of Sciences, USA 85, 5315–19.Google Scholar
Takemoto, T. (1978). Isolation and structural identification of naturally occurring excitatory amino acids. In Kainic Acid as a Tool in Neurobiology (ed., McGeer, E. G., Olney, J. W. & McGeer, P.), pp. 1–15. New York: Raven Press.Google Scholar
Walrond, J. P., Kass, I. S., Stretton, A. O. W. & Donmoyer, J. E. (1985). Identification of excitatory and inhibitory motorneurons in the nematode Ascaris by electrophysiological techniques. Journal of Neuroscience 5, 1–8.Google Scholar
Walrond, J. P. & Stretton, A. O. W. (1985A). RECIPROCAL INHIBITION IN the motor nervous system of the nematode Ascaris: direct control of ventral inhibitory motorneurons by dorsal excitatory motorneurons. Journal of Neuroscience 5, 9–15.Google Scholar
Walrond, J. P. & Stretton, A. O. W. (1985b). Excitatory and inhibitory activity in the dorsal musculature of the nematode Ascaris evoked by single dorsal excitatory motoneurons. Journal of Neuroscience 5, 16–22.Google Scholar
Wang, B. (1996). Diverse actions of FMRFamide-like neuropeptides on muscle cells and neuromuscular transmission of the nematode Ascaris suum. MSc. thesis, University of Wisconsin, Madison.Google Scholar
White, J. G., Albertson, D. G. & Anness, M. A. R. (1978). Connectivity changes in a class of motorneurons during the development of a nematode. Nature 271, 764–6.Google Scholar
White, J. G., Southgate, E., Thomson, J. N. & Brenner, s. (1976). The structure of the ventral nerve cord of Caenorhabditis elegans. Philosophical Transactions of the Royal Society of London B 275, 327–48.Google Scholar
White, J. G., Southgate, E., Thomson, J. N. & Brenner, s. (1986). The structure of the nervous system of Caenorhabditis elegans. Philosophical Transactions of the Royal Society of London B 314, 1–340.Google Scholar