Neuromechanics of multifunctionality during rejection in Aplysia californica

How are the same muscles and neurons used to generate qualitatively different behaviors? We studied this question by analyzing the biomechanical and neural mechanisms of rejection responses in the marine mollusk Aplysia californica and compared these mechanisms with those used to generate swallowing responses (Ye et al., 2006). During rejection, the central grasper of the feeding structure closes to push inedible food out of the buccal cavity. This contrasts with swallowing, during which the grasper is open as it moves toward the jaws (protracts). We examined how the shape change of the grasper during rejection mechanically reconfigured the surrounding musculature. Grasper shape change increased the effectiveness of protractor muscle I2. The closed grasper alters the function of another muscle, the hinge, which becomes capable of inducing ventral rotations of rejected material. In contrast, during large-amplitude swallows, the hinge muscle mediates dorsal rotations of ingested material. Finally, after the grasper opens, its change in shape induces a delay in the activation of other surrounding muscles, the I1/I3/jaw complex, whose premature activation would close the halves of the grasper and induce it to pull inedible material back inward. The delay in activation of the I1/I3/jaw complex is partially attributable to identified multiaction neurons B4/B5. The results suggest that multifunctionality emerges from a periphery in which flexible coalitions of muscles may perform different functions in different mechanical contexts and in which neural circuitry is capable of reorganizing to exploit these coalitions by changes in phasing, duration, and intensity of motor neuronal activation.