Mechanical reconfiguration mediates swallowing and rejection in Aplysia californica

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.

Motor neuronal activity varies least among individuals when it matters most for behavior

“…As the I2 muscle is activated it shortens, and thus it loses mechanical advantage and its force is reduced because of its length/tension property (Neustadter et al 2007;Novakovic et al 2006;Sutton et al 2004;Yu et al 1999). Closure of the grasper changes the grasper shape from roughly spherical to roughly ellipsoidal (compare Fig.…”

“…Closure of the grasper changes the grasper shape from roughly spherical to roughly ellipsoidal (compare Fig. 6, top, 2nd and 3rd panels), elongating the I2 muscle and thus enhancing I2's ability to protract (Neustadter et al 2007;Novakovic et al 2006).…”

“…Consequently, any single DOF deployed as part of a combination may be less correlated with motor output than if it were deployed alone. For example, there are tradeoffs on how soon the grasper should close to enhance protraction [too early, and the closed grasper cannot grasp food; too late, and it provides no assistance to I2 (Novakovic et al 2006)]. Many combinations may be essentially equivalent; thus I2/RN overlap may not correlate strongly with behavioral efficacy.…”

Neuromechanics of Multifunctionality during Rejection inAplysia californica

“…Because we established many of the neural and biomechanical mechanisms that underlie swallowing responses of different amplitude in the marine mollusk Aplysia californica (Ye et al, 2006), we sought to determine how these properties changed during a qualitatively different behavior, rejection. Magnetic resonance (MR) imaging showed that the central grasper (radula/odontophore) changes shape from spherical when it is open to ellispsoidal when it is closed (Neustadter et al, 2002b;Novakovic et al, 2006). We hypothesized that grasper shape change may alter the shapes and positions of surrounding muscles, and this mechanical reconfiguration is crucial for the neural control of rejection (Novakovic et al, 2006).…”

“…Magnetic resonance (MR) imaging showed that the central grasper (radula/odontophore) changes shape from spherical when it is open to ellispsoidal when it is closed (Neustadter et al, 2002b;Novakovic et al, 2006). We hypothesized that grasper shape change may alter the shapes and positions of surrounding muscles, and this mechanical reconfiguration is crucial for the neural control of rejection (Novakovic et al, 2006).…”