Incorporating buccal mass planar mechanics and anatomical features improves neuromechanical modeling ofAplysiafeeding behavior
Authors: Bennington Michael J. , Liao Ashlee S. , Sukhnandan Ravesh , Kundu Bidisha , Rogers Stephen M. , Gill Jeffrey P. , McManus Jeffrey M. , Sutton Gregory P. , Chiel Hillel J. , Webster-Wood Victoria A. 
Published: September 2024

To understand how behaviors arise in animals, it is necessary to investigate both the neural circuits and the biomechanics of the periphery. A tractable model system for studying multifunctional control is the feeding apparatus of the marine molluskAplysia californica. Previousin silicoandin robotomodels have investigated how the nervous and muscular systems interact in this system. However, these models are still limited in their ability to matchin vivodata both qualitatively and quantitatively. We introduce a new neuromechanical model ofAplysiafeeding that combines a modified version of a previously developed neural model with a novel biomechanical model that better reflects the anatomy and kinematics ofAplysiafeeding. The model was calibrated using a combination of previously measured biomechanical parameters and hand-tuning to behavioral data. Using this model, simulation feeding experiments were conducted, and the resulting behavioral metrics were compared to animal data. The model successfully produces three key behaviors seen inAplysiaand demonstrates a good quantitative agreement with biting and swallowing behaviors. Additional work is needed to match rejection behavior quantitatively and to reflect qualitative observations related to the relative contributions of two key muscles, the hinge and I3. Future improvements will focus on incorporating the effects of deformable 3D structures in the simulated buccal mass.

Author summary

Animals need to produce a wide array of behaviors so that they can adapt to changes in their environment. To understand how behaviors are performed, we need to understand how the brain and the body work together in their environment. One tractable system in which to study this brain-body relationship is the feeding behavior of the sea slugAplysia californica. Despite having a small fraction of the number of neurons that humans have, this animal can produce many behaviors, respond to a changing environment, and learn from previous experiences. We have create an improved computer model of the slug’s mouthparts that simulates many of its key muscles and the forces they produce, together with a representation of the network of neurons that control them. With this model, we can recreate the feeding behaviors that we observe in the real animal, including biting, swallowing, and rejection, and use it to make quantitative predictions of how the animal will behave and respond to different stimuli. We found however that some aspects of the system were not well represented by simple 1-dimensional muscles, as has been done in most biomechanical models to date, but requires us to consider more complicated deformations of these soft bodies. Using this model as a tool, we aim to test hypotheses about brain-body interactions in the sea slug to better understand the behavior of small, slowly moving animals.