Locomotion grows up: The neuromechanical control of interlimb coordinating mechanisms in crayfish

Locomotion Grows Up: The Neuromechanical Control of Interlimb Coordinating Mechanisms in Crayfish Marc D. Rinehart Locomotion requires many dynamic interactions between organism and environment at several levels. It is not known how the nervous system controls all of these relationships to ultimately produce and guide locomotor behavior. Furthermore, it is not known whether the nervous system needs to recognize and control all of the possible body-environment interactions. In this study the crayfish (Procambarus clarkii) is used as a model system to test how size influences locomotor behavior and how a single, simplified neuromechanical system can accommodate these changes. A set of behavioral experiments was conducted to characterize kinematics of freely walking juvenile crayfish to compare with adults. The purpose of these studies was to determine how crayfish adapt to a great change in size during their ontogeny. Juvenile and adult crayfish show differences in limb function and coordination. Although crayfish are decapods, the juveniles predominantly use the posterior legs and behave more like four-legged walkers. The difference in locomotor behavior can best be explained by differences in chelae size. Allometric relationships between juveniles and adults show limb and body morphologies scale proportionately. Adult chelae, or claws, are twice as long and contribute ~20% more to the total body mass in fully mature crayfish. This increase in chelae size shifts the location of the center of mass anterior as crayfish grow. The result is a change in relative load distribution that appears to affect individual limb behavior and interlimb coordination. Shifting the center of mass in adults by amputating the chelae resulted in limb behavior and interlimb coordination more similar to that observed in juveniles. Likewise, applying load to the rostrum of juveniles altered behavior and changed limb function in the posterior legs similar to adults with large chelae. The results of these experiments suggest that crayfish of all sizes adapt to changes in load distribution by adjusting behavior of individual legs. To test whether developmental influences have an effect on walking behavior, juveniles were induced to walk on a treadmill at various speeds. The animals showed more consistent limb coordination as walking speed increased, similar to adults. Selected legs were then amputated to test how gait was affected. Amputating legs removes sensory feedback from the distal leg to the central nervous system. The behavior of the stump is therefore more representative of the endogenous rhythmicity of the central pattern generator (CPG). Juveniles showed no differences in coordination in individual legs. Coordination between adjacent ipsilateral legs was also the same as that observed in adults following amputation. Furthermore, intact legs acquired new interlimb coordination similar to adults. These results suggested that juvenile and adult crayfish have functionally similar nervous systems controlling walking. Finally, a 3-D virtual crayfish was built to test whether differences in walking between juveniles and adults could be due to mechanical influences alone. The model crayfish lacked direct connections between legs. The model responded to shifts in the center of mass by showing more consistent limb coordination in those legs nearest the center of mass. This was achieved through indirect mechanical coupling of the legs through the environment and body of the crayfish. This mechanism also produced realistic adaptive behavior when limbs were amputated. This showed that differences between adult and juvenile walking are due solely to mechanical influences associated with the changing center of mass as the animals grow. These results suggest further that organisms do not need high levels of control to produce coordinated behavior. Locomotor behavior arises through interactions between body, limb, and environment that are a function of the spatio-temporal dynamics of body morphology. The results may be applicable to a large number of walking systems.