Context-dependent mechanical reconfiguration is necessary for multifunctional behavior in a constrained hydrostat

Authors

Bennington, M. J., Rogers, S. M., Neustadter, D. M., Quinn, R. D., Sutton, G. P., Chiel, H. J., Webster-Wood, V. A.

Abstract

Muscular hydrostats, muscular structures with no rigid skeleton, are ubiquitous within the animal kingdom, from vertebrate tongues to cephalopod arms, but how they perform complex actions remains poorly understood. One model hydrostat studied for its neural control and biomechanics is the feeding system (buccal mass) of the sea hare Aplysia (Fig. 1). The buccal mass (Fig. 1b) performs multiple feeding behaviors by coordinating intrinsic muscles to move a grasper (odontophore). In this paper, we investigated how mechanical reconfiguration from interacting shape-changing elements facilitates large odontophore protractions. During rejection behaviors, mechanical reconfiguration of the odontophore (elongating its shape to a higher aspect ratio) stretches a protractor muscle (I2), allowing I2 to generate stronger protractions. In biting behaviors, the odontophore has a similar range of motion. However, during biting, the odontophore has a lower aspect ratio throughout protraction, meaning the I2 muscle alone is insufficient to reach observed protractions due to its length/tension property and reduced mechanical advantage. By combining new analysis of MRI movies of Aplysia feeding (Fig. 1) with a new biomechanical model for biting and rejection (Fig. 2), we demonstrate two context-dependent mechanical reconfiguration mechanisms that explain the different ways large protractions are produced in biting and rejection (Fig. 3). The mechanisms integrate shape changes, bending and conforming of muscle structures, and shifts in contact interactions. We propose two mechanical subclasses of muscular hydrostats, "constrained" or "unconstrained" (Fig. 4), that may be morphologically similar but employ different control strategies depending on whether mechanical constraints are reliably present.

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The authors list and abstract were imported from bioRxiv on 06 Apr 2026.

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