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Neural control exploits changing mechanical advantage and context dependence to generate different feeding responses in Aplysia

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Abstract.

How does neural control reflect changes in mechanical advantage and muscle function? In the Aplysia feeding system a protractor muscle’s mechanical advantage decreases as it moves the structure that grasps food (the radula/odontophore) in an anterior direction. In contrast, as the radula/odontophore is moved forward, the jaw musculature’s mechanical advantage shifts so that it may act to assist forward movement of the radula/odontophore instead of pushing it posteriorly. To test whether the jaw musculature’s context-dependent function can compensate for the falling mechanical advantage of the protractor muscle, we created a kinetic model of Aplysia’s feeding apparatus. During biting, the model predicts that the reduction of the force in the protractor muscle I2 will prevent it from overcoming passive forces that resist the large anterior radula/odontophore displacements observed during biting. To produce protractions of the magnitude observed during biting behaviors, the nervous system could increase I2’s contractile strength by neuromodulating I2, or it could recruit the I1/I3 jaw muscle complex. Driving the kinetic model with in vivo EMG and ENG predicts that, during biting, early activation of the context-dependent jaw muscle I1/I3 may assist in moving the radula/odontophore anteriorly during the final phase of protraction. In contrast, during swallowing, later activation of I1/I3 causes it to act purely as a retractor. Shifting the timing of onset of I1/I3 activation allows the nervous system to use a mechanical equilibrium point that allows I1/I3 to act as a protractor rather than an equilibrium point that allows I1/I3 to act as a retractor. This use of equilibrium points may be similar to that proposed for vertebrate control of movement.

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Author information

Author notes

  1. David M. Neustadter

    Present address: Elbit Systems Ltd., Haifa, Israel, 31053

Authors and Affiliations

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

    Gregory P. Sutton & Elizabeth V. Mangan

  2. Case Western Reserve University, Department of Biomedical Engineering, Cleveland, OH, USA

    David M. Neustadter, Patrick E. Crago & Hillel J. Chiel

  3. Case Western Reserve University, Department of Electrical Engineering and Computer Science, Cleveland, OH, USA

    Randall D. Beer

  4. Case Western Reserve University, Departments of Biology and Neurosciences, 2080 Adelbert Road, Cleveland, OH, 44106-7080, USA

    Hillel J. Chiel

Authors
  1. Gregory P. Sutton
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  2. Elizabeth V. Mangan
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  3. David M. Neustadter
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  4. Randall D. Beer
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  5. Patrick E. Crago
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  6. Hillel J. Chiel
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Corresponding author

Correspondence to Hillel J. Chiel.

Additional information

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. We would also 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.

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Sutton, G., Mangan, E., Neustadter, D. et al. Neural control exploits changing mechanical advantage and context dependence to generate different feeding responses in Aplysia. Biol. Cybern. 91, 333–345 (2004). https://doi.org/10.1007/s00422-004-0517-z

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  • DOI: https://doi.org/10.1007/s00422-004-0517-z

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