Biophysical Journal 22: 349-372 (1978)
© 1978 the Biophysical Society

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The Pumping Mechanism of the Nematode Esophagus

ABSTRACT

The radial orientation of the myofilaments in the nematode esophagus raises interesting questions as to how such a structure can function as a pump. A physical model of the esophagus of Ascaris lumbricoides was developed and the membrane theory of shells applied in order to relate the observed dimensional changes to myofilament force, pressure stresses, and membrane elastic constants. By stressing the excised esophagus passively with osmotic pressure, the esophagus was shown to be elastically anisotropic with the ratio of circumferential to longitudinal elastic constants, E/E_l 2.74. When this value was incorporated, the model predicted the ratio of the respective strains, /_l, to be 0.52 during an equilibrium contraction of the esophagus. This agreed with the experimental value, 0.46 ± 0.10, measured during occasional, prolonged muscle contractions. When measured during normal pumping, on the other hand, the value of /_l was 0 ± 0.10. This indicated that a nonequilibrium condition normally occurs in which a greater myofilament force per unit area of lumen membrane is not balanced by internal pressure and therefore acceleration of the lumen contents and negative intraluminal pressure occurs.

The pumping action of esophagi dissected from Ascaris was observed to be normally peristaltic and periodic. Contraction was initiated by a spontaneous depolarization that propagated at 4.0 ± 0.20 cm/s along the esophageal membrane. A wave of localized increases in the internal pressure of the muscle and localized changes in external dimensions was observed. A subsequent spontaneous repolarization, which propagated at 5.8 ± 0.23 cm/s, triggered relaxation of the muscle during which the localized pressure and dimensional changes returned to resting values. A mechanism was deduced in which fluid is drawn into and moved along the lumen by the wave of contraction. During the wave of relaxation, the lumen contents are pressurized and injected into the intestine by elastic restoring forces.