Functional subdivision of fin protractor and retractor muscles underlies pelvic fin walking in the African lungfish (Protopterus annectens)

Abstract

African lungfish Protopterus annectens can produce rotational movements around the joint between the pelvis and the pelvic fin, allowing these animals to walk across benthic substrates. In tetrapods, limb rotation at the hip joint is a common feature of substrate-based locomotion. For sprawling tetrapods, rotation can involve nine or more muscles, which are often robust and span multiple joints. In contrast, P. annectens uses a modest morphology of two fan-shaped muscles, the pelvic fin protractor and retractor, to accomplish this movement. We hypothesized that functional subdivision, coupled with their broad insertions on the femur, allows each of these muscles to pull on the limb from multiple directions and provides a mechanism for fin rotation. To test this hypothesis, we examined the muscle activity at three locations in both the protractor and the retractor muscles during walking. Electromyograms show differences in the timing of muscle activation between dorsal and ventral regions of each muscle, suggesting that each muscle is functionally subdivided once. The subdivisions demonstrate sequential onsets of muscle activity and overlap of activity between regions, which are also features of limb control in tetrapods. These data indicate that subdivisions of protractor and retractor muscles impart functional complexity to a morphologically simple system, and suggest a mechanism that allows lungfish to produce a tetrapod-like walking gait with only two muscles. As one of few extant sarcopterygian fishes, P. annectens may provide important functional data to inform interpretation of limb movement of fossil relatives.

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

“…EMG electrodes were constructed using 0.005 mm diameter bifilar, insulated (nylon bond coat, annealed) stainless steel wire (California Fine Wire, Grover Beach, CA) that was bared 0.5 mm on one end, fed through a 26 gauge syringe needle, and formed into a twist‐hook for muscle implantation (Aiello, King, & Hale, 2014; Herrel et al, 2008; Loeb & Gans, 1986). All electrodes were centrally wired to an Omnetics 27 pin male circular connector (Part No.…”

“…Animals were anesthetized using Ketamine (10 mg/kg). Electrodes for muscle recordings were implanted percutaneously into the right and left leg of each individual following published methods (Aiello et al, 2014; Herrel et al, 2008; Loeb & Gans, 1986). In each leg, two bipolar EMG electrodes were implanted in m. peroneus longus and another two in mm.…”

Dynamic Musculoskeletal Functional Morphology: Integrating diceCT and XROMM

“…Morphological and functional heterogeneity can also be found within muscles in the form of variable activation patterns, fiber lengths, pennation, and fiber types. Muscles with simple morphology can thus be functionally subdivided to achieve more complex movements (Aiello et al, 2014). In muscles with regional disparity in fiber-type distribution, the orderly recruitment of smaller, slow-twitch fibers prior to larger, fast-twitch fibers in both locomotor and feeding musculature (Henneman et al, 1965;Milner-Brown et al, 1973;Goldberg and Derfler, 1977;Yemm, 1977;Clark et al, 1978;Mendell, 2005;Ross et al, 2007Ross et al, , 2010 probably results in portions of muscles with different lengths, maximum velocities, forces, and moment arm lengths becoming active prior to others (Higham and Biewener, 2011).…”

Fins into limbs: Recent insights from sarcopterygian fish

“…Tetrapods, however, use nine or more muscles during their walking gait, whereas lungfish possess only two fan‐shaped muscle masses that link the femur to the pelvis. Using electromyogram to record muscle activity, Aiello, King, and Hale () showed that lungfish use ventral and dorsal regions of its fin protractor and retractor muscles to lift the body from the substrate and produce a tetrapod‐like walking gait.…”