The organization of movement is a complex and difficult problem, in part because of a "degrees of freedom problem" in motor control. The richness of an animal's movement possibilities makes its choice of movement controls complex. However, unlike current robots, animals cope efficiently with their degrees of freedom. A newborn wildebeest calf walks with the herd within a few hours of birth. A frog or a turtle, using just its spinal cord, can control complex goal-directed trajectories. The spinal cord can also rapidly correct such movements if they are perturbed. It has been argued that these remarkable capacities are modular, constructed with small sets of primitives or motor building blocks. How such primitives arise and are used is the focus of this project.
The concepts of modularity and motor primitives have provided useful descriptions of the organization of spinal motor systems. Modular organization has been shown to support spinal behaviors, and may help to "bootstrap" motor learning. Nonetheless, modularity is controversial at many levels. Spinal primitives might need to be supplanted or augmented in order to perform complex, voluntary behaviors. This project attacks this problem in frog prey strike behaviors, a voluntary and adapted behavior in a system that is fundamentally important to the animal, and has also been well characterized in previous studies of modularity. The neuromechanics of prey strike is examined from a multi-disciplinary perspective. The importance of modular organization in neuroscience and behavior extends well beyond biological motor control, with ramifications in evolutionary and cognitive psychology. Biological strategies and solutions are also highly relevant to future technologies and robotics.
A computer model of prey strike will be developed using a novel approach based on Cosserat strand-elements. The model will be developed by a team of four investigators: Simon Giszter (neurophysiology) and Jonathan Nissanov (anatomy, imaging) at Drexel University, Dinesh Pai (computer science, biomechanical modeling) at the University of British Columbia, and Kiisa Nishikawa (neuromechanics) at Northern Arizona University. Cryoplane microscopy will be used to reconstruct bullfrog sensorimotor anatomy in detail. These structures will be modeled using a strand-based approach to incorporate this detail. Experimental and model analyses of prey strike using these data will inform one another to establish the benefits and limits of fixed or adaptive modular mechanisms, and the biological implementation used in frogs.
Overview: Our project explores the basic organization of movement in the spinal cord. Limb movements made to lift a glass, kick a football, dance a jig or play a musical instrument must all operate through the spinal cord. The spinal contains the 'final common path' to the muscles. Our project has examined spinal cord using the idea that the spinal cord cord contains a set of building blocks - termed motor primitives- that are used to construct movement. Fairly similar spinal organization, pattern generation and motor primitives appear to underlie movement organized in frog, rat, cat and even human spinal cords. Motor primitives were first described in frogs, and our project uses frogs to explore how they are used in movement. We here examined the frog's prey strike behavior - which is of fundamental importance to a frog's survival in the wild. A main finding of this work is a strong role of spinal motor primitives in constructing this voluntary behavior. Broader Impacts: Motor primitives are of broad importance and interest as a way of building movement. During the funding period we have disseminated our results in Engineering and Neurology journals as well as in basic neuroscience publications. The ideas explored here are broadly useful for understanding issues in human movement and rehabilitation after injury, and may impact design of biomimetic robots and technologies. In the course of the work significant training and educational opportunities have been provided. In summers we have hosted high school interns, undergraduate bioengineers and medical student trainees who have aided us as research staff, enhancing scientific education and understanding, and educating them in a range of laboratory and interdisciplinary skills. The project has also supported two doctoral graduate students thus training the next generation of active scientists. The project is formed of collaborations among three Universities, two in the US and one in Canada, hence enhancing scientific collaboration nationally and internationally. Overall the project has thus had broad impacts on neuroscience, education, academia, and technology. Intellectual Merit: Our data show that the brain of the frog uses the spinal primitives to construct the leaps used to capture food. During these behaviors, spinal motor primitives are rather like the keys on a piano, or the notes in a musical score that is used by the brain. It is suggested that by sequencing primitives (i.e., by the ‘score’) and combining primitives (i.e., by choosing the ‘chords’) basic motions can be built. The motor primitives in the spinal cord act as a spinal 'instrument' for the brain. We found that each leg is controlled individually as a separate 'instrument', even in jumps using both legs. In such movements, the brain 'orchestrates' the various motor primitives to achieve a graceful and well coordinated jump to its target, and a precise prey capture. The frog prey strike is considerably more sophisticated than often supposed. Frogs strike with their tongue while their body is moving and turning as they leap toward their prey. This is a feat more or less equivalent to a person accurately firing a crossbow or pistol at a nearby rabbit, as they travel through the air after leaping off a diving board. Despite the precision and sophistication of the feat, the frog's prey strike is largely composed by using the spinal building blocks. In addition, our work has raised new questions about the ways in which this 'musical score' of motor primitives is actively assembled and adapted to circumstances, and provided pilot 'signposts' as to how this might be discovered next. This new knowledge of spinal mechanisms is likely to be of broad significance. To better understand the spinal building blocks we have also built computer simulations of the muscles and skeleton of the frog. This is a central part of the collaboration between labs in Pennsylvania (Giszter, Drexel), Arizona (Nishikawa, NAU) and Canada (Pai, UBC). The computer simulations show that conventional ways of simulating muscle are not sufficient. To describe the tongue strike in the frog, new ideas about muscle behavior from the experiments of Nishikawa must be added. These 'next generation' muscle models get closer to the motion performance observed. The new muscle models extend our understanding of muscles and of energy storage in muscle. The results can improve our understanding of the great efficiency of animals as 'movement machines', and may help inform future robot technology. Summary: In summary, our project has produced fundamental new knowledge about how brains build and control movements using the spinal cord resources and limb properties, and about muscle as a machine. In obtaining this new knowledge numerous trainees from the high school to doctoral level have participated in an international and national interdisciplinary scientific collaboration. They have leaned new techniques and ways of thinking. Our results have been disseminated broadly to the basic scientific, engineering and medical communities.
