Relating neuromuscular control to functional anatomy of limb muscles in extant archosaurs

• Published in: Journal of morphology (1931) Vol. 280; no. 5; pp. 666 - 680
• Main Authors: Cuff, Andrew R., Daley, Monica A., Michel, Krijn B., Allen, Vivian R., Lamas, Luis Pardon, Adami, Chiara, Monticelli, Paolo, Pelligand, Ludo, Hutchinson, John R.
• Format: Journal Article
• Language: English
• Published: Hoboken, USA John Wiley & Sons, Inc 01.05.2019; Wiley Blackwell (John Wiley & Sons)
• Subjects: Animals; Birds - anatomy & histology; Birds - physiology; Electromyography; evolution; Extinction, Biological; Extremities - anatomy & histology; Extremities - physiology; locomotion; morphology; Muscle, Skeletal - anatomy & histology; Muscle, Skeletal - physiology; musculoskeletal system; neural control; Neuromuscular Junction - physiology; Reptiles - anatomy & histology; Reptiles - physiology; Signal Processing, Computer-Assisted; Time Factors; musculoskeletal system; neural control; evolution; morphology; locomotion
• ISSN: 0362-2525; 1097-4687; 1097-4687
• DOI: 10.1002/jmor.20973

Electromyography (EMG) is used to understand muscle activity patterns in animals. Understanding how much variation exists in muscle activity patterns in homologous muscles across animal clades during similar behaviours is important for evaluating the evolution of muscle functions and neuromuscular control. We compared muscle activity across a range of archosaurian species and appendicular muscles, including how these EMG patterns varied across ontogeny and phylogeny, to reconstruct the evolutionary history of archosaurian muscle activation during locomotion. EMG electrodes were implanted into the muscles of turkeys, pheasants, quail, guineafowl, emus (three age classes), tinamous and juvenile Nile crocodiles across 13 different appendicular muscles. Subjects walked and ran at a range of speeds both overground and on treadmills during EMG recordings. Anatomically similar muscles such as the lateral gastrocnemius exhibited similar EMG patterns at similar relative speeds across all birds. In the crocodiles, the EMG signals closely matched previously published data for alligators. The timing of lateral gastrocnemius activation was relatively later within a stride cycle for crocodiles compared to birds. This difference may relate to the coordinated knee extension and ankle plantarflexion timing across the swing‐stance transition in Crocodylia, unlike in birds where there is knee flexion and ankle dorsiflexion across swing‐stance. No significant effects were found across the species for ontogeny, or between treadmill and overground locomotion. Our findings strengthen the inference that some muscle EMG patterns remained conservative throughout Archosauria: for example, digital flexors retained similar stance phase activity and M. pectoralis remained an ‘anti‐gravity’ muscle. However, some avian hindlimb muscles evolved divergent activations in tandem with functional changes such as bipedalism and more crouched postures, especially M. iliotrochantericus caudalis switching from swing to stance phase activity and M. iliofibularis adding a novel stance phase burst of activity. Our results show that there are ancestral patterns of muscle activity in Archosauria Modern crocodilians maintain these ancestral patterns, while modern birds evolved divergent activations particularly in M. iliotrochantericus caudalis and M. iliofibularis.