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

Abstract

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. K E Y W O R D S evolution, locomotion, morphology, musculoskeletal system, neural control

Testing the propulsive role of m. peroneus longus during quadrupedal walking in Varanus exanthematicus

“…In fact, the only species that shows an unusual muscle activation pattern are veiled chameleons (Higham & Jayne, 2004), which is likely due to this species’ highly arboreal lifestyle (Boyer et al, 2007; Kingston et al, 2010). These data from phylogenetically and anatomically disparate lizard species speak to the conserved nature of motor patterns during locomotion (Cuff et al, 2019; Goslow, Dial & Jenkins, 1989; Lauder & Shaffer, 1988; Peters & Goslow, 1983; Wainwright, Sanford, Reilly, & Lauder, 1989). Considering the sprawling posture and limb kinematics shared between many squamates (Granatosky et al, 2019b), it is possible that m. peroneus longus may have a minor role in propulsion even in species without an enlarged lateral calcaneal heel (Reilly, 1995), although the propulsive moment arm of the muscle would be smaller.…”

“…Thus, the propulsive role of m. peroneus longus in V. exanthematicus was probably built upon existing muscle activity patterns present in ancestral squamates and then exaggerated through modifications to lateral calcaneal heel and the associated proximal expansion of the fifth metatarsal (Sullivan, 2010). Phylogenetic studies in the style of Cuff et al (2019) could further elucidate this hypothesis.…”

“…Finally, a series of regression analyses were used to determine whether the activity patterns of m. peroneus longus behaves like another known powerful propulsive muscle of the ankle (i.e., mm. gastrocnemii; Cuff et al, 2019; Reilly, 1995). All statistical tests were performed in MATLAB.…”

“…However, Sullivan (2010) argued that for species moving with a sprawling gait a lateral calcaneal heel, and the associated proximal expansion of the fifth metatarsal, could allow m. peroneus longus to function as a powerful propulsive muscle along with mm. gastrocnemii and m. flexor digitorum longus (Cuff et al, 2019; Reilly, 1995; Sullivan, 2010).…”

Perioperative pharmacokinetics and pharmacodynamics of meloxicam in emus (Dromaius novaehollandiae) of different age groups using nonlinear mixed effect modelling

“…The emus in this study were anaesthetised during a biomechanical ratite study for surgical implantation of bone strain gauges and electromyogram wires (Cuff et al., 2019; Main & Biewener, 2007). The study was approved by the Royal Veterinary College Clinical Research (CRERB approval number: CR2018‐006‐2) and Ethics and Welfare Research boards.…”