Passive hinge forces in the feeding apparatus of Aplysia aid retraction during biting but not during swallowing

Abstract

Swallowing and biting responses in the marine mollusk Aplysia are both mediated by a cyclical alternation of protraction and retraction movements of the grasping structure, the radula and underlying odontophore, within the feeding apparatus of the animal, the buccal mass. In vivo observations demonstrate that Aplysia biting is associated with strong protractions and rapid initial retractions, whereas Aplysia swallowing is associated with weaker protractions and slower initial retractions. During biting, the musculature joining the radula/odontophore to the buccal mass (termed the "hinge") is stretched more than in swallowing. To test the hypothesis that stretch of the hinge might contribute to rapid retractions observed in biting, we analyzed the hinge's passive properties. During biting, the hinge is stretched sufficiently to assist retraction. In contrast, during swallowing, the hinge is not stretched sufficiently for its passive forces to assist retraction, because the odontophore's anterior movement is smaller than during biting. A quantitative model demonstrated that steady-state passive forces were sufficient to generate the retraction movements observed during biting. Experimental measures of the relative magnitude of the hinge's active and passive forces at the protraction displacements of biting suggest that passive forces are at least a third of the total force.

Neuromechanics of Coordination during Swallowing inAplysia californica

“…The minimum stretch of the hinge at which B7 could begin to exert force was 0.35 Ϯ 0.02 buccal mass lengths (n ϭ 4). These values were similar to the maximum hinge stretch during swallowing estimated from in vivo magnetic resonance images (Sutton et al, 2004a). C, During carbachol-induced feeding motor programs, B7 strongly depolarizes and fires action potentials at the same time that the tube moves inward and rotates dorsally.…”

“…The grasper itself consists of a cartilaginous surface covered by fine teeth (referred to as the radula), which is controlled by underlying muscles (referred to as the odontophore) that open and close the grasper. The grasper rotates about a hinge muscle, which consists of the interdigitation of the muscle fibers of several major muscles of the grasper itself and the muscles surrounding the grasper (Sutton et al, 2004a). Protraction is mediated by the I2 muscle, whose motor neurons are B31, B32, B61, and B62 (Hurwitz et al, 1996).…”

“…Activating B7 caused no rotation of the tube. In general, B7 had no effect when the hinge was stretched to a length near the minimum hinge stretch estimated from in vivo magnetic resonance images of swallows (Sutton et al, 2004a). The experiment was repeated four times at an average stretch of 0.21 Ϯ 0.03 buccal mass lengths, and activating B7 had no effect in any of these experiments.…”

“…A, Top shows a schematic diagram of the peak protraction of a type A swallow. Based on previous in vitro studies (Sutton et al, 2004a), hinge stretch was estimated from the position of the tip of the odontophore. In the experiment shown in the bottom, the hinge was stretched to 0.19 buccal mass lengths.…”

Neuromechanics of Multifunctionality during Rejection inAplysia californica

“…Grasper shape change increases the strength of protractor muscle I2 (the intrinsic muscle 2). The muscle around which the grasper rotates, known as the "hinge" (Sutton et al, 2004a), can induce ventral rotations attributable to the closure of the grasper during protraction. Grasper shape change also induces a delay in activating the muscle complex that moves the grasper back toward the esophagus (the I1/I3/jaw complex) to allow the grasper to remain open and release inedible material.…”