Robustness, flexibility, and sensitivity in a multifunctional motor control model

Abstract

Motor systems must adapt to perturbations and changing conditions both within and outside the body. We refer to the ability of a system to maintain performance despite perturbations as “robustness,” and the ability of a system to deploy alternative strategies that improve fitness as “flexibility.” Different classes of pattern-generating circuits yield dynamics with differential sensitivities to perturbations and parameter variation. Depending on the task and the type of perturbation, high sensitivity can either facilitate or hinder robustness and flexibility. Here we explore the role of multiple coexisting oscillatory modes and sensory feedback in allowing multiphasic motor pattern generation to be both robust and flexible. As a concrete example, we focus on a nominal neuromechanical model of triphasic motor patterns in the feeding apparatus of the marine mollusk Aplysia californica. We find that the model can operate within two distinct oscillatory modes and that the system exhibits bistability between the two. In the “heteroclinic mode,” higher sensitivity makes the system more robust to changing mechanical loads, but less robust to internal parameter variations. In the “limit cycle mode,” lower sensitivity makes the system more robust to changes in internal parameter values, but less robust to changes in mechanical load. Finally, we show that overall performance on a variable feeding task is improved when the system can flexibly transition between oscillatory modes in response to the changing demands of the task. Thus, our results suggest that the interplay of sensory feedback and multiple oscillatory modes can allow motor systems to be both robust and flexible in a variable environment.