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Passive hinge forces in the feeding apparatus of Aplysia aid retraction during biting but not during swallowing

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Abstract

Swallowing and biting responses in the marine mollusk Aplysia are both mediated by a cyclical alternation of protraction and retraction movements of the grasping structure, the radula and underlying odontophore, within the feeding apparatus of the animal, the buccal mass. In vivo observations demonstrate that Aplysia biting is associated with strong protractions and rapid initial retractions, whereas Aplysia swallowing is associated with weaker protractions and slower initial retractions. During biting, the musculature joining the radula/odontophore to the buccal mass (termed the “hinge”) is stretched more than in swallowing. To test the hypothesis that stretch of the hinge might contribute to rapid retractions observed in biting, we analyzed the hinge’s passive properties. During biting, the hinge is stretched sufficiently to assist retraction. In contrast, during swallowing, the hinge is not stretched sufficiently for its passive forces to assist retraction, because the odontophore’s anterior movement is smaller than during biting. A quantitative model demonstrated that steady-state passive forces were sufficient to generate the retraction movements observed during biting. Experimental measures of the relative magnitude of the hinge’s active and passive forces at the protraction displacements of biting suggest that passive forces are at least a third of the total force.

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Fig. 1A–C
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Fig. 3. A
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Fig. 11A, B

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Abbreviations

I1/I3:

intrinsic buccal muscles 1 and 3

I2:

intrinsic buccal muscle 2 (nomenclature from Howells 1942)

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Acknowledgements

The authors would like to thank Dr. Joseph Mansour for his help with data analysis and his comments on an earlier draft of the manuscript. The authors would also like to thank Elizabeth Mangan for early work on a previous design of the experimental apparatus, and Robert Herman for his help in providing outlines of the buccal mass and radular stalk (Fig. 2). In addition, we would like to thank Dr. Richard Drushel for his anatomical illustrations of the buccal mass (Fig. 1). This work was supported by NSF grants IBN9974394 and IBN0218386, NSF IGERT grant 345-1898, and HHMI grant 71199600606. All experiments comply with the laws of the United States of America.

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Authors and Affiliations

  1. Department of Mechanical and Aerospace Engineering, Case Western Reserve University, Cleveland, OH, 44106-7080, USA

    G. P. Sutton & G. P. Sunny

  2. Department of Biological Basis of Behavior, University of Pennsylvania, Pennsylvania, USA

    J. B. Macknin

  3. Department of Biomedical Engineering, Case Western Reserve University, Cleveland, OH, 44106-7080, USA

    S. S. Gartman, P. E. Crago & D. M. Neustadter

  4. Elbit Systems Ltd., 31053, Haifa, Israel

    D. M. Neustadter

  5. Department of Electrical Engineering and Computer Science, Case Western Reserve University, Cleveland, OH, 44106-7080, USA

    R. D. Beer

  6. Department of Biology, Case Western Reserve University, 2080 Adelbert Road, Cleveland, OH, 44106-7080, USA

    H. J. Chiel

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  1. G. P. Sutton
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  2. J. B. Macknin
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  3. S. S. Gartman
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  4. G. P. Sunny
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  7. D. M. Neustadter
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  8. H. J. Chiel
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Correspondence to H. J. Chiel.

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Sutton, G.P., Macknin, J.B., Gartman, S.S. et al. Passive hinge forces in the feeding apparatus of Aplysia aid retraction during biting but not during swallowing. J Comp Physiol A 190, 501–514 (2004). https://doi.org/10.1007/s00359-004-0517-4

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  • DOI: https://doi.org/10.1007/s00359-004-0517-4

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