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Microelectrode studies of the tegument and sub-tegumental compartments of male Schistosoma mansoni: an analysis of electrophysiological properties

Published online by Cambridge University Press:  06 April 2009

D. P. Thompson
Affiliation:
Departments of Zoology, and Pharmacology and Toxicology, Michigan State University, East Lansing, Michigan 48824
R. A. Pax
Affiliation:
Departments of Zoology, and Pharmacology and Toxicology, Michigan State University, East Lansing, Michigan 48824
J. L. Bennett
Affiliation:
Departments of Zoology, and Pharmacology and Toxicology, Michigan State University, East Lansing, Michigan 48824

Summary

Standard intracellular microelectrode techniques were used to determine the electrical properties of the tegument and sub-tegumental regions in male Schistosoma mansoni. Three distinct compartments of electrical potential were observed. The resting potentials recorded in these compartments of –45·9±2·5 mV (Eteg), –22·0±1·1 mV (E2) and – 4·7±0·3 mV (E3) corroborate those previously reported by Fetterer, Pax & Bennett (1980) and Bricker, Pax & Bennett (1981). Input resistance was measured in each compartment and was found to be 4·5 MΩ (tegument), 9·2 MΩ (E2) and 3·5 MΩ (E3). Time-constants for the tegument, E2 and E3 were 0·24±0·01 msec, 0·25±0·01 msec and 0·13±0·01 msec, respectively. Multiple electrode experiments revealed that the tegument and E2 compartment are electrical syncytia with similar current-spreading capabilities. Low resistance pathways also appear to connect the tegument and E2 region, since electrotonic signals initiated in either of those compartments experience only a 15–25% reduction upon passing into the other. Injecting large (> 200 nA) depolarizing current pulses into the tegument or E2 compartment often resulted in the initiation of active membrane responses. These spikes were highly variable, ranging from 4 to 75 mV in magnitude (occasionally overshooting zero potential by as much as 25 mV) and from 10–40 msec in duration. The responses were not actively propagated along the parasite, and their decay over distance was approximately equal to that predicted on the basis of length constant values obtained from electrotonic signals. The addition of a non-diffusible solute to the recording medium resulted in a significant reduction in the current-spreading capacity of both the tegument and E2 compartment. Coupling ratios between the tegument and E2 compartment were decreased, and the input resistance for both compartments increased, while resting potentials remained constant. Active responses could not be evoked in schistosomes exposed to the hyperosmotic medium.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1982

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References

Araki, T. & Otani, T. (1955). Response of single motorneurons to direct stimulation in toad's spinal cord. Journal of Neurophysiology 18, 472–85.CrossRefGoogle Scholar
Bricker, C. S., Pax, R. A. & Bennett, J. L. (1981). Characterization of subtegumental compartments of male Schistosoma mansoni using intracellular techniques. Journal of Parasitology (in the Press).Google Scholar
Bricker, C. S., Pax, R. A. & Bennett, J. L. (1982). Microelectrode studies of the tegument and sub-tegumental compartments of male Schistosoma mansoni: anatomical location of sources of electrical potentials. Parasitology 85, 149–61.Google Scholar
Caveney, S. (1974). Intercellular communication in a positional field: Movement of small ions between insect epidermal cells. Developmental Biology 40, 311–22.Google Scholar
Fetterer, R. H., Pax, R. A. & Bennett, J. L. (1977). Schistosoma mansoni: Direct method for simultaneous recordings of the electrical and motor activity. Experimental Parasitology 43, 286–94.CrossRefGoogle ScholarPubMed
Fetterer, R. H., Pax, R. A. & Bennett, J. L. (1980). Schistosoma mansoni: Characterization of the electrical potential from the tegument of adult males. Experimental Parasitology 49, 353–65.CrossRefGoogle ScholarPubMed
Frank, K. & Fourtes, G. F. (1956). Stimulation of spinal motorneurons with intracellular electrodes. Journal of Physiology 134, 451–70.Google Scholar
Hirst, G. D. S. & Neild, T. O. (1978). An analysis of excitatory junctional potentials recorded from arterioles. Journal of Physiology 280, 87104.CrossRefGoogle ScholarPubMed
Hodgkin, A. L. & Rushton, W. A. H. (1946). The electrical constants of a crustacean nerve fibre. Proceedings of the Royal Society, London 133, 444–79.Google Scholar
Jack, J. J. B., Noble, D. & Tsien, R. W. (1975). Electrical Flow in Excitable Cells. Oxford: Clarendon.Google Scholar
Kriebel, M. E. (1968). Electrical characteristics of the tunicate heart cell membrane and nexuses. Journal of General Physiology 52, 4659.Google Scholar
Matricon-Gondran, M. (1980). Gap junctions and particle aggregates in the tegumentary syncytium of a trematode. Tissue and Cell 12, 383–94.Google Scholar
Mekata, F. (1971). Electrophysiological studies of the smooth muscle cell membrane of the rabbit common carotid artery. Journal of General Physiology 57, 738–51.Google Scholar
Pax, R. A., Bennett, J. L. & Fetterer, R. H. (1978). A benzodiazepine derivative and praziquantel: Effects on musculature of Schistosoma mansoni and Schistosoma japonicum. Naunyn Schmiedeberg's Archives of Pharmacology 304, 309–15.CrossRefGoogle ScholarPubMed
Shiba, H. (1971). Heaviside's ‘bessel cable’ as an electric model for flat simple epithelial cells with low resistive junctional membranes. Journal oj Theoretical Biology 30, 5968.CrossRefGoogle ScholarPubMed
Silk, M. H., Spence, I. M. & Gear, J. H. S. (1969 a). Ultrastructural studies of the blood fluke: Schistosoma mansoni. I. The integument. South African Journal of Medical Science 34, 110.Google ScholarPubMed
Silk, M. H. & Spence, I. (1969 b). Ultrastructural studies on the blood fluke S. mansoni. II. The musculature. South African Journal of Medical Science 34, 1128.Google Scholar
Tomita, T. (1966). Electrical responses of smooth muscle to external stimulation in hypertonic solution. Journal of Physiology 183, 450–68.Google Scholar
Tomita, T. (1967). Current spread in the smooth muscle of the guinea-pig vas deferens. Journal of Physiology 189, 163–76.Google Scholar
Woodbury, J. W. & Crill, W. E. (1961). On the problem of impulse conduction in the atrium. In Nervous Inhibition, pp. 426. Oxford: Pergamon.Google Scholar