Molluscs are adapted to a broad range of environmental niches and feed on a wide range of foods with varying biomechanical properties (Brusca and Brusca, 1990). The molluscan feeding apparatus is characterized by a rasping surface (the radula) and an underlying muscular structure (the odontophore) that is often associated with a cartilaginous structure (bolsters or rotellae; Starmühlner, 1956). A variety of different hypotheses have been proposed to account for the function of these structures. For example, investigators have proposed that the radular surface and underlying odontophore might act like a pulley, a block and tackle, a rasp or a conveyer belt (Eales, 1921; Howells, 1942; Smith, 1988). These hypotheses have been based on observations of the parts of the structure visible during portions of the feeding cycle, histological characterizations of the anatomy and stimulation of individual muscles. For example, careful kinematic analysis of radular kinetics during grazing in Helisoma trivolvis indicated that the radula slides over the underlying cartilage, which is independently accelerated during each feeding stroke, supporting a moving conveyor belt hypothesis (Smith, 1988). Analysis of the radula and odontophore within the buccal mass is complicated by the absence of hard skeletal elements and discrete joints that make musculo-skeletal systems tractable to mechanical analysis. Molluscan feeding structures are composed entirely of muscle and cartilage, and muscle acts both to generate forces and to provide skeletal support. Thus, they are examples of a broader class of structures, muscular hydrostats, that are exemplified by tongues, trunks and tentacles (Kier and Smith, 1985). Because these structures have many degrees of freedom and are thus capable of complex and flexible movements, understanding their biomechanical properties is likely to be essential for a deeper understanding of their neural control. Moreover, the great flexibility of these structures allows them to be utilized for multiple different behavioral functions (e.g. the human tongue is used both for feeding and for talking), and thus the neural architectures controlling these devices are also of special interest for understanding the dynamics of multifunctionality. We have focused on analyzing the biomechanics and neural control of feeding in the marine mollusc Aplysia californica. Aplysia is a generalist herbivore that feeds on a variety of red, brown and green seaweeds whose shapes, toughness and texture vary significantly (Carefoot, 1967; Howells, 1942; 3177 The Journal of Experimental Biology 205, 3177–3206 (2002) Printed in Great Britain © The Company of Biologists Limited 2002 JEB4290 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. Movies available on-line Key words: feeding, behaviour, biomechanics, kinematics, mollusc, muscular hydrostat, Aplysia californica. Summary Introduction A kinematic model of swallowing in Aplysia californica based on radula/odontophore kinematics and in vivo magnetic resonance images David M. Neustadter 1,4 , Richard F. Drushel 2 , Patrick E. Crago 1 , Benjamin W. Adams 2 and Hillel J. Chiel 1–3, * Departments of 1 Biomedical Engineering, 2 Biology and 3 Neurosciences, Case Western Reserve University, Cleveland, OH 44106-7080, USA and 4 MR Systems Department, G. E. Medical Systems Israel Ltd, Keren Hayesod Street, PO Box 2071, Tirat Carmel 39120, Israel *Author for correspondence at address 2 (e-mail: hjc@po.cwru.edu) Accepted 3 July 2002