Mechanical reconfiguration mediates swallowing and rejection in Aplysia californica

Muscular hydrostats, such as tongues, trunks or tentacles, have fewer constraints on their degrees of freedom than musculoskeletal systems, so changes in a structure’s shape may alter the positions and lengths of other components (i.e., induce mechanical reconfiguration). We studied mechanical reconfiguration during rejection and swallowing in the marine mollusk Aplysia californica. During rejection, inedible material is pushed out of an animal’s buccal cavity. The grasper (radula/odontophore) closes on inedible material, and then a posterior muscle, I2, pushes the grasper toward the jaws (protracts it). After the material is released, an anterior muscle complex (the I1/I3/jaw complex) pushes the grasper toward the esophagus (retracts it). During swallowing, the grasper is protracted open, and then retracts closed, pulling in food. Grasper closure changes its shape. Magnetic resonance images show that grasper closure lengthens I2. A kinetic model quantified the changes in the ability of I2 and I1/I3 to exert force as grasper shape changed. Grasper closure increases I2’s ability to protract during rejection, and increases I1/I3’s ability to retract during swallowing. Motor neurons controlling radular closure may therefore affect the behavioral outputs of I2’s and I1/I3’s motor neurons. Thus, motor neurons may modulate the outputs of other motor neurons through mechanical reconfiguration.Valerie A. Novakovic and Gregory P. Sutton contributed equally to the paper.