Person:

Kawai, Risa

To navigate different environments, an animal must be able to adapt its locomotory gait to its physical surroundings. The nematode Caenorhabditis elegans, between swimming in water and crawling on surfaces, adapts its locomotory gait to surroundings that impose approximately 10,000-fold differences in mechanical resistance. Here we investigate this feat by studying the undulatory movements of C. elegans in Newtonian fluids spanning nearly five orders of magnitude in viscosity. In these fluids, the worm undulatory gait varies continuously with changes in external load: As load increases, both wavelength and frequency of undulation decrease. We also quantify the internal viscoelastic properties of the worm’s body and their role in locomotory dynamics. We incorporate muscle activity, internal load, and external load into a biomechanical model of locomotion and show that (i) muscle power is nearly constant across changes in locomotory gait, and (ii) the onset of gait adaptation occurs as external load becomes comparable to internal load. During the swimming gait, which is evoked by small external loads, muscle power is primarily devoted to bending the worm’s elastic body. During the crawling gait, evoked by large external loads, comparable muscle power is used to drive the external load and the elastic body. Our results suggest that C. elegans locomotory gait continuously adapts to external mechanical load in order to maintain propulsive thrust.

Addressing the neural mechanisms underlying complex learned behaviors requires training animals in well-controlled tasks, an often time-consuming and labor-intensive process that can severely limit the feasibility of such studies. To overcome this constraint, we developed a fully computer-controlled general purpose system for high-throughput training of rodents. By standardizing and automating the implementation of predefined training protocols within the animal’s home-cage our system dramatically reduces the efforts involved in animal training while also removing human errors and biases from the process. We deployed this system to train rats in a variety of sensorimotor tasks, achieving learning rates comparable to existing, but more laborious, methods. By incrementally and systematically increasing the difficulty of the task over weeks of training, rats were able to master motor tasks that, in complexity and structure, resemble ones used in primate studies of motor sequence learning. By enabling fully automated training of rodents in a home-cage setting this low-cost and modular system increases the utility of rodents for studying the neural underpinnings of a variety of complex behaviors.

Motor skill learning underlies much of what we do, be it hitting a tennis serve, playing the piano, or simply brushing our teeth. Yet despite its importance, little is known about the neural circuits that implement the learning process or how the motor program is represented in the brain. Here I explore the role of motor cortex through lesion studies in rats trained on a motor skill. First, I interrogate whether motor cortex is necessary for the production of a complex motor sequence by training animals to produce temporally precise self-initiated movement sequences on a lever-pressing task. The movement sequences that emerged over months of training were remarkably complex, yet very precise. This motor skill, once mastered, survives large bilateral motor cortex lesions, suggesting that motor cortex is not required for generating movement sequences after consolidation. Next, I explored the role of motor cortex in motor skills that require dexterous manipulations. Animals trained to make constrained spatially precise movements using a joystick were impaired after motor cortex lesions. The role of motor cortex thus depends on the nature of the movements involved but not on the sequencing of movements. Third, I explored the function of motor cortex in sensorimotor transformations by training animals on the same lever-pressing task but with external cues instead of self-initiated movement. Surprisingly, these animals were also not impaired after lesions, suggesting that the method of learning the motor sequence has no consequence once the motor sequences are consolidated. Lastly, I explored the role of motor cortex in learning motor skills. Animals that were lesioned after being exposed to the lever-pressing task could learn to adjust the timing of their movements, indicating that motor cortex is not required for adapting a previously-acquired motor sequence. Lesions of motor cortex prior to any training, however, severely disrupted learning. Even with extended training, animals were unable to fully master the task, demonstrating that motor cortex is necessary for the acquisition of new motor skills even when it is not required for their execution.