Soft-surface grasping: radular opening in Aplysia californica.

Grasping soft, irregular material is challenging both for animals and robots. The feeding systems of many animals have adapted to this challenge. In particular, the feeding system of the marine mollusk Aplysia californica, a generalist herbivore, allows it to grasp and ingest seaweeds of varying shape, texture and toughness. On the surface of the grasper of A. californica is a structure known as the radula, a thin flexible cartilaginous sheet with fine teeth. Previous in vitro studies suggested that intrinsic muscles, I7, are responsible for opening the radula. Lesioning I7 in vivo does not prevent animals from grasping and ingesting food. New in vitro studies demonstrate that a set of fine muscle fibers on the ventral surface of the radula - the sub-radular fibers (SRFs) - mediate opening movements even if the I7 muscles are absent. Both in vitro and in vivo lesions demonstrate that removing the SRFs leads to profound deficits in radular opening, and significantly reduces feeding efficiency. A theoretical biomechanical analysis of the actions of the SRFs suggests that they induce the radular surface to open around a central crease in the radular surface and to arch the radular surface, allowing it to softly conform to irregular material. A three-dimensional model of the radular surface, based on in vivo observations and magnetic resonance imaging of intact animals, provides support for the biomechanical analysis. These results suggest how a soft grasper can work during feeding, and suggest novel designs for artificial soft graspers.

The kinematics of multifunctionality: comparisons of biting and swallowing in Aplysia californica.

What are the mechanisms of multifunctionality, i.e. the use of the same peripheral structures for multiple behaviors? We studied this question using the multifunctional feeding apparatus of the marine mollusk Aplysia californica, in which the same muscles mediate biting (an attempt to grasp food) and swallowing (ingestion of food). Biting and swallowing responses were compared using magnetic resonance imaging of intact, behaving animals and a three-dimensional kinematic model. Biting is associated with larger amplitude protractions of the grasper (radula/odontophore) than swallowing, and smaller retractions. Larger biting protractions than in swallowing appear to be due to a more anterior position of the grasper as the behavior begins, a larger amplitude contraction of protractor muscle I2, and contraction of the posterior portion of the I1/I3/jaw complex. The posterior I1/I3/jaw complex may be context-dependent, i.e. its mechanical context changes the direction of the force it exerts. Thus, the posterior of I1/I3 may aid protraction near the peak of biting, whereas the entire I1/I3/jaw complex acts as a retractor during swallowing. In addition, larger amplitude closure of the grasper during swallowing allows an animal to exert more force as it ingests food. These results demonstrate that differential deployment of the periphery can mediate multifunctionality.

A kinematic model of swallowing in Aplysia californica based on radula/odontophore kinematics and in vivo magnetic resonance images.

A kinematic model of the buccal mass of Aplysia californica during swallowing has been developed that incorporates the kinematics of the odontophore, the muscular structure that underlies the pincer-like grasping structure, the radula. The model is based on real-time magnetic resonance images (MRIs) of the mid-sagittal cross section of the buccal mass during swallowing. Using kinematic relationships derived from isolated odontophores induced to perform feeding-like movements, the model generates predictions about movement of the buccal mass in the medio-lateral dimension during the feeding cycle that are well-matched to corresponding coronal MRIs of the buccal mass during swallowing. The model successfully reproduces changes in the lengths of the intrinsic (I) buccal muscles I2 and I3 measured experimentally. The model predicts changes in the length of the radular opener muscle I7 throughout the swallowing cycle, generates hypotheses about the muscular basis of radular opening prior to the onset of forward rotation during swallowing and suggests possible context-dependent functions for the I7 muscle, the radular stalk and the I5 (ARC) muscle during radular opening and closing.

Radula-centric and odontophore-centric kinematic models of swallowing in Aplysia californica.

Two kinematic models of the radula/odontophore of the marine mollusc Aplysia californica were created to characterize the movement of structures inside the buccal mass during the feeding cycle in vivo. Both models produce a continuous range of three-dimensional shape changes in the radula/odontophore, but they are fundamentally different in construction. The radulacentric model treats the radular halves as rigid bodies that can pitch, yaw and roll relative to a fixed radular stalk, thus creating a three-dimensional shape. The odontophore-centric model creates a globally convex solid representation of the radula/odontophore directly, which then constrains the positions and shapes of internal structures. Both radula/odontophore models are placed into a pre-existing kinematic model of the I1/I3 and I2 muscles to generate three-dimensional representations of the entire buccal mass. High-temporal-resolution, mid-sagittal magnetic resonance (MR) images of swallowing adults in vivo are used to provide non-invasive, artifact-free shape and position parameter inputs for the models. These images allow structures inside the buccal mass to be visualized directly, including the radula, radular stalk and lumen of the I1/I3 cavity. Both radula-centric and odontophore-centric models were able to reproduce two-dimensional, mid-sagittal radula/odontophore and buccal mass kinematics, but the odontophore-centric model's predictions of I1/I3, I2 and I7 muscle dimensions more accurately matched data from MR-imaged adults and transilluminated juveniles.

Kinematics of the buccal mass during swallowing based on magnetic resonance imaging in intact, behaving Aplysia californica.

A novel magnetic resonance imaging interface has been developed that makes it possible to image movements in intact, freely moving subjects. We have used this interface to image the internal structures of the feeding apparatus (i.e. the buccal mass) of the marine mollusc Aplysia californica. The temporal and spatial resolution of the resulting images is sufficient to describe the kinematics of specific muscles of the buccal mass and the internal movements of the main structures responsible for grasping food, the radula and the odontophore. These observations suggest that a previously undescribed feature on the anterior margin of the odontophore, a fluid-filled structure that we term the prow, may aid in opening the jaw lumen early in protraction. Radular closing during swallowing occurs near the peak of protraction as the radular stalk is pushed rapidly out of the odontophore. Retraction of the odontophore is enhanced by the closure of the lumen of the jaws on the elongated odontophore, causing the odontophore to rotate rapidly towards the esophagus. Radular opening occurs after the peak of retraction and without the active contraction of the protractor muscle 12 and is due, in part, to the movement of the radular stalk into the odontophore. The large variability between responses also suggests that the great flexibility of swallowing responses may be due to variability in neural control and in the biomechanics of the ingested food and to the inherent flexibility of the buccal mass.