The feeding behavior of the marine mollusc Aplysia californica is an intensively studied model system for understanding the neural control of behavior. Feeding movements are generated by contractions of the muscles of the buccal mass. These muscles are internal and cannot be visualized during behavior. In order to infer the movements of the muscles of the buccal mass, two kinematic models were constructed. The first kinematic model assumed that the complex consisting of the pincer-like radula and the underlying odontophore was spherical in shape. In this model, the radula/odontophore was moved anteriorly or posteriorly and the more superficial buccal muscles (I1/I3 and I2) were fitted around it. Although the overall buccal mass shapes predicted by this model were similar to those observed in vivo during protraction, the shapes predicted during retraction were very different. We therefore constructed a second kinematic model in which the shape of the radula/odontophore was based on the shapes assumed by those structures in vitro when they were passively forced into protraction, rest or retraction positions. As each of these shapes was rotated, the second kinematic model generated overall shapes of the buccal mass that were similar to those observed in vivo during swallowing and tearing, and made predictions about the antero-posterior length of the buccal mass and the relative location of the lateral groove. These predictions were consistent with observations made in vivo and in vitro. The kinematic patterns of intrinsic buccal muscles I1 and I2 in vivo were estimated using the second model. Both models make testable predictions with regard to the functions and neural control of intrinsic buccal muscles I2 and I3.
Changes in the positions, shapes and movements of the feeding apparatus (buccal mass) of the marine mollusc Aplysia californica were studied in intact, transilluminated juveniles. The buccal mass assumes characteristic shapes as its internal structure, the radula/odontophore, moves anteriorly (protracts) or posteriorly (retracts). These shapes are especially distinctive when the radula/odontophore has protracted forwards fully, is close to its resting or neutral position, or has retracted backwards fully. We refer to the shapes that occur at full protraction, transition and full retraction as shape 1 (spherical), shape 2 (ovoid) and shape 3 (gamma-shaped), respectively. We introduce this shape nomenclature in order to avoid confusion with the existing terms protraction and retraction, which we reserve exclusively to describe the direction of movement of the radula/odontophore. The observed shape changes do not agree with those predicted on the basis of in vitro observations of a feeding head preparation, but are similar to shapes observed in vitro in the snail Lymnaea stagnalis. The buccal mass also rotates approximately 10 degrees dorsally during retraction, pivoting on the attachment to the mouth, before the subsequent protraction and return of the buccal mass to the transition shape. This rotation may be due to activation of the extrinsic muscles of the buccal mass. Plots of the buccal mass shape parameters eccentricity versus ellipticity create a two-dimensional shape space, which accurately quantifies the subtle transitions of shape between the different phases of the feeding cycle. Quantitative differences are observed between pure swallows and swallows with tearing behavior, but the qualitative shapes are similar. Hysteresis in the shape space plots of most swallows provides evidence for the hypothesis that protraction and retraction each have distinct 'active' and 'return' phases. The observed kinematic pattern imposes constraints on the internal structures of the buccal mass and may be used to infer the shape and positions of the radula and odontophore.