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First published online January 8, 2007
Journal of Experimental Biology 210, 238-260 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02654

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

David M. Neustadter^1,*, Robert L. Herman², Richard F. Drushel³, David W. Chestek¹ and Hillel J. Chiel^3,4,1,

¹ Department of Biomedical Engineering, Case Western Reserve University, Cleveland, OH 44106, USA
² Department of Electrical Engineering and Computer Science, Case Western Reserve University, Cleveland, OH 44106, USA
³ Department of Biology, Case Western Reserve University, Cleveland, OH 44106, USA
⁴ Department of Neurosciences, Case Western Reserve University, Cleveland, OH 44106, USA

Author for correspondence (e-mail: hjc{at}case.edu)

Accepted 7 November 2006

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.

Key words: feeding behavior, biomechanics, kinematics, mollusk, muscular hydrostat

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