Precocious Locomotor Behavior Begins in the Egg: Development of Leg Muscle Patterns for Stepping in the Chick

BACKGROUND: The chicken is capable of adaptive locomotor behavior within hours after hatching, yet little is known of the processes leading to this precocious skill. During the final week of incubation, chick embryos produce distinct repetitive limb movements that until recently had not been investigated. In this study we examined the leg muscle patterns at 3 time points as development of these spontaneous movements unfolds to determine if they exhibit attributes of locomotion reported in hatchlings. We also sought to determine whether the deeply flexed posture and movement constraint imposed by the shell wall modulate the muscle patterns. METHODOLOGY/PRINCIPAL FINDINGS: Synchronized electromyograms for leg muscles, force and video were recorded continuously from embryos while in their naturally flexed posture at embryonic day (E) 15, E18 and E20. We tested for effects of leg posture and constraint by removing shell wall anterior to the foot. Results indicated that by E18, burst onset time distinguished leg muscle synergists from antagonists across a 10-fold range in burst frequencies (1–10 Hz), and knee extensors from ankle extensors in patterns comparable to locomotion at hatching. However, burst durations did not scale with step cycle duration in any of the muscles recorded. Despite substantially larger leg movements after shell removal, the knee extensor was the only muscle to vary its activity, and extensor muscles often failed to participate. To further clarify if the repetitive movements are likely locomotor-related, we examined bilateral coordination of ankle muscles during repetitive movements at E20. In all cases ankle muscles exhibited a bias for left/right alternation. CONCLUSIONS/SIGNIFICANCE: Collectively, the findings lead us to conclude that the repetitive leg movements in late stage embryos are locomotor-related and a fundamental link in the establishment of precocious locomotor skill. The potential importance of differences between embryonic and posthatching locomotion is discussed.