Neuromechanics of Coordination during Swallowing inAplysia californica

Abstract

Bernstein (1967) hypothesized that preparation of the periphery was crucial for correct responses to motor output. To test this hypothesis in a behaving animal, we examined the roles of two identified motor neurons, B7 and B8, which contribute to feeding behavior in the marine mollusk Aplysia californica. Neuron B7 innervates a hinge muscle and has no overt behavioral effect during smaller-amplitude (type A) swallows, because the hinge muscle is too short to exert force. Neuron B8 activates a muscle (I4) that acts solely to grasp material during type A swallows. During larger-amplitude (type B) swallows, the behavioral actions of both motor neurons change, because the larger-amplitude anterior movement of the grasper sets up the periphery to respond differently to motor outputs. The larger anterior movement stretches the hinge muscle, so that activating neuron B7 mediates the initial retraction phase of swallowing. The changed position of the I4 muscle allows neuron B8 not only to induce grasping but also to pull material into the buccal cavity, contributing to retraction. Thus, larger-amplitude swallows are associated with the expression of two new degrees of freedom (use of the hinge to retract and use of the grasper to retract) that are essential for mediating type B swallows. These results provide a direct demonstration of Bernstein's hypothesis that properly positioning the periphery can be crucial for its ability to correctly respond to motor output and also demonstrate that biomechanical context can alter the functions of identified motor neurons.

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

“…It is clear that many bites and many swallows occupy distinct locations in the space defined by their motor components, but it is also clear that there is some overlap. This is not surprising, because we have previously shown that swallows may have variants with different strengths of protraction, making them more similar to bites (Ye et al 2006a).…”

“…To characterize the key motor features, we determined the start and stop times of the I2 EMG during the protraction phase by measuring both the time of the first spike and the time at which the muscle EMG reached 10 Hz and the stop time when it fell below 5 Hz (Hurwitz et al 1996; 3 measures), the start and stop times of the largest units on RN (corresponding to activity in the B8a/b neurons; Chiel 1993a, 1993b; 2 measures), the start and stop times of the B4/B5 units on BN3 [largest units on BN3 (Warman and Chiel 1995) from the first to the last spike; 2 measures], and the start and stop times of identified motor neurons B6/B9 and B43 (Lu et al 2013;4 measures). Finally, we measured the third-largest units on BN2 (Church and Lloyd 1994;Morton and Chiel 1993b;Ye et al 2006a), focusing on when they began in retraction (1 measure), for a total of 12 different measures of the motor program. The start and end times of other features of the motor pattern that were absent in many motor patterns were noted but were not used further for the analysis in this report: activity in motor neuron B3 (largest extracellular unit on BN2), bursts of activity in B4/B5 above 40 Hz, the third largest unit on BN2 in the protraction phase, activity of motor neuron B38 in protraction, and activity of motor neuron B38 in retraction.…”

“…An analysis of the role of motor neuron B38 during swallowing can be found in McManus et al (2014). We attempted to determine the start and stop times of smaller units on BN3 [since among them would be the motor neurons B15/B16 (Cropper et al 1990) and B7 (Ye et al 2006a)] but found that their sizes were too similar to be reliably distinguished. Therefore, we did not analyze them further.…”

“…Once again, the B4/B5 AUC value falls within the region of significance. movements (Neustadter et al 2002a(Neustadter et al , 2007, computer simulation of the kinematics (Neustadter et al 2002b(Neustadter et al , 2007 and kinetics (Sutton et al 2004) of the behaviors, characterization of motor patterns for variants of swallowing (Ye et al 2006a), and studies of biting and swallowing in a reduced, semi-intact preparation (McManus et al 2012). Thus it is possible to define biomechanical features that are likely to discriminate between the two behaviors.…”

Neuromechanics of Multifunctionality during Rejection inAplysia californica

“…Multifunctionality is difficult to study, because it is hard to simultaneously characterize biomechanics and neural control. 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).…”