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Mechanical reconfiguration mediates swallowing and rejection in Aplysia californica

  • Original Paper
  • Published:
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Abstract

Muscular hydrostats, such as tongues, trunks or tentacles, have fewer constraints on their degrees of freedom than musculoskeletal systems, so changes in a structure’s shape may alter the positions and lengths of other components (i.e., induce mechanical reconfiguration). We studied mechanical reconfiguration during rejection and swallowing in the marine mollusk Aplysia californica. During rejection, inedible material is pushed out of an animal’s buccal cavity. The grasper (radula/odontophore) closes on inedible material, and then a posterior muscle, I2, pushes the grasper toward the jaws (protracts it). After the material is released, an anterior muscle complex (the I1/I3/jaw complex) pushes the grasper toward the esophagus (retracts it). During swallowing, the grasper is protracted open, and then retracts closed, pulling in food. Grasper closure changes its shape. Magnetic resonance images show that grasper closure lengthens I2. A kinetic model quantified the changes in the ability of I2 and I1/I3 to exert force as grasper shape changed. Grasper closure increases I2’s ability to protract during rejection, and increases I1/I3’s ability to retract during swallowing. Motor neurons controlling radular closure may therefore affect the behavioral outputs of I2’s and I1/I3’s motor neurons. Thus, motor neurons may modulate the outputs of other motor neurons through mechanical reconfiguration.

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Abbreviations

I2:

Intrinsic buccal muscle 2

I1/I3:

Intrinsic buccal muscles 1 and 3

LT:

Length/tension

FI2:

Force in I2

Fmax:

Maximum force

BML:

Buccal mass lengths

B8a,b, B61, B62, B63:

Buccal ganglion motor neurons and interneurons

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Acknowledgements

We thank the NSF (IBN-0218386 to HJC) and the NIH (NS-047073 to HJC), and the NSF IGERT program (Grant 345–1898) for their support of this research. We also thank Richard Drushel for the illustration of the buccal mass anatomy (Fig. 1a), and for his helpful comments on the research in this paper, and Robert Herman for his sketches of the MRI. Experiments described in this study comply with the Principles of animal care, publication No. 86-23, revised 1985, of the National Institute of Health, and also with the current laws of the United States.

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Author notes

  1. Valerie A. Novakovic

    Present address: Veterans Administration Boston Healthcare System, 1400 VFW Parkway Building 3, Room 2A110, West Roxbury, MA, 02132, USA

  2. David M. Neustadter

    Present address: , Ruth Hamoavia 3, Apt. 3, Netanya, 42756, Israel

Authors and Affiliations

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

    Valerie A. Novakovic, Randall D. Beer & Hillel J. Chiel

  2. Department of Mechanical and Aerospace Engineering, Case Western Reserve University, 10900 Euclid Avenue, 44106-7222, Cleveland, OH, USA

    Gregory P. Sutton

  3. Department of Biomedical Engineering, Case Western Reserve University, 319 Wickendon Building, 10900 Euclid Avenue, 44106-7207, Cleveland, OH, USA

    David M. Neustadter & Hillel J. Chiel

  4. Department of Electrical Engineering and Computer Science, Case Western Reserve University, 10900 Euclid Avenue, 44106-7071, Cleveland, OH, USA

    Randall D. Beer

  5. Department of Neurosciences School of Medicine, Case Western Reserve University, 2109 Adelbert Road, 44106-4975, Cleveland, OH, USA

    Hillel J. Chiel

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  1. Valerie A. Novakovic
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Corresponding author

Correspondence to Hillel J. Chiel.

Additional information

Valerie A. Novakovic and Gregory P. Sutton contributed equally to the paper.

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Novakovic, V.A., Sutton, G.P., Neustadter, D.M. et al. Mechanical reconfiguration mediates swallowing and rejection in Aplysia californica . J Comp Physiol A 192, 857–870 (2006). https://doi.org/10.1007/s00359-006-0124-7

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