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

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.

Radula-centric and odontophore-centric kinematic models of swallowing in Aplysia californica.

Two kinematic models of the radula/odontophore of the marine mollusc Aplysia californica were created to characterize the movement of structures inside the buccal mass during the feeding cycle in vivo. Both models produce a continuous range of three-dimensional shape changes in the radula/odontophore, but they are fundamentally different in construction. The radulacentric model treats the radular halves as rigid bodies that can pitch, yaw and roll relative to a fixed radular stalk, thus creating a three-dimensional shape. The odontophore-centric model creates a globally convex solid representation of the radula/odontophore directly, which then constrains the positions and shapes of internal structures. Both radula/odontophore models are placed into a pre-existing kinematic model of the I1/I3 and I2 muscles to generate three-dimensional representations of the entire buccal mass. High-temporal-resolution, mid-sagittal magnetic resonance (MR) images of swallowing adults in vivo are used to provide non-invasive, artifact-free shape and position parameter inputs for the models. These images allow structures inside the buccal mass to be visualized directly, including the radula, radular stalk and lumen of the I1/I3 cavity. Both radula-centric and odontophore-centric models were able to reproduce two-dimensional, mid-sagittal radula/odontophore and buccal mass kinematics, but the odontophore-centric model's predictions of I1/I3, I2 and I7 muscle dimensions more accurately matched data from MR-imaged adults and transilluminated juveniles.