Rapid Adaptation to Changing Mechanical Load by Ordered Recruitment of Identified Motor Neurons

As they interact with their environment and encounter challenges, animals adjust their behavior on a moment-to-moment basis to maintain task fitness. This dynamic process of adaptive motor control occurs in the nervous system, but an understanding of the biomechanics of the body is essential to properly interpret the behavioral outcomes. To study how animals respond to changing task conditions, we used a model system in which the functional roles of identified neurons and the relevant biomechanics are well understood and can be studied in intact behaving animals: feeding in the marine mollusc Aplysia. We monitored the motor neuronal output of the feeding circuitry as intact animals fed on uniform food stimuli under unloaded and loaded conditions, and we measured the force of retraction during loaded swallows. We observed a previously undescribed pattern of force generation, which can be explained within the appropriate biomechanical context by the activity of just a few key, identified motor neurons. We show that, when encountering load, animals recruit identified retractor muscle motor neurons for longer and at higher frequency to increase retraction force duration. Our results identify a mode by which animals robustly adjust behavior to their environment, which is experimentally tractable to further mechanistic investigation.