Motor patterns and kinematics during backward walking in the Pacific Giant Salamander: Evidence for novel motor output

Kinematic and motor patterns during forward and backward walking in the salamander Dicamptodon tenebrosus were compared to determine whether the differences seen in mammals also apply to a lower vertebrate with sprawling posture and to measure the flexibility of motor output by tetrapod central pattern generators. During treadmill locomotion, electromyograms (EMGs) were recorded from hindlimb muscles of Dicamptodon while simultaneous high-speed video records documented movement of the body, thigh, and crus and allowed EMGs to be synchronized to limb movements. In forward locomotion, the trunk was lifted above the treadmill surface. The pelvic girdle and trunk underwent smooth side-to-side oscillations throughout the stride. At the beginning of the stance phase, the femur was protracted and the knee joint extended. The knee joint initially flexed in early stance and then extended as the foot pushed off in late stance, reaching maximum extension just before foot lift-off The femur retracted steadily throughout the stance. In the swing phase, the femur rapidly protracted, and the leg was brought forward in an "overhand crawl" motion. In backward walking, the body frequently remained in contact with the treadmill surface. The pelvic girdle, trunk, and femur remained relatively still during stance phase, and most motion occurred at the knee joint. The knee joint extended throughout most of stance, as the body moved back, away from the stationary foot. The knee flexed during swing. Four of five angles showed significantly smaller ranges in backward than in forward walking. EMGs of forward walking showed that ventral muscles were coactive, beginning activity just before foot touchdown and ceasing during the middle of stance phase. Dorsal muscles were active primarily during swing. Backward locomotion showed a different pattern; all muscles except one showed primary activity during the swing phase. This pattern of muscle synergy in backward walking never was seen in forward locomotion. Also, several muscles demonstrated lower burst rectified integrated areas (RIA) or durations during backward locomotion. Multivariate statistical analysis of EMG onset and RIA completely separated forward and backward walking along the first principal component, based on higher RIAs, longer durations of muscle activity, and greater synergy between ventral muscles during early stance in forward walking. Backward walking in Dicamptodon uses a novel motor pattern not seen during forward walking in salamanders or during any other locomotor activity in previously studied tetrapods. The central neuronal mechanisms mediating locomotion in this primitive tetrapod are thus capable of considerable plasticity.