Anticipatory motor patterns limit muscle stretch during landing in toads

Abstract

To safely land after a jump or hop, muscles must be actively stretched to dissipate mechanical energy. Muscles that dissipate energy can be damaged if stretched to long lengths. The likelihood of damage may be mitigated by the nervous system, if anticipatory activation of muscles prior to impact alters the muscle's operating length. Anticipatory motor recruitment is well established in landing studies and motor patterns have been shown to be modulated based on the perceived magnitude of the impact. In this study, we examine whether motor recruitment in anticipation of landing can serve a protective function by limiting maximum muscle length during a landing event. We use the anconeus muscle of toads, a landing muscle whose recruitment is modulated in anticipation of landing. We combine in vivo measurements of muscle length during landing with in vitro characterization of the force-length curve to determine the muscle's operating length. We show that muscle shortening prior to impact increases with increasing hop distance. This initial increase in muscle shortening functions to accommodate the larger stretches required when landing after long hops. These predictive motor strategies may function to reduce stretch-induced muscle damage by constraining maximum muscle length, despite variation in the magnitude of impact.

Forelimb kinematics during hopping and landing in toads (Bufo marinus)

“…If forelimbs are extended more in longer hops, as is suggested by the Azizi and Abbott (2013) strain data, this could be the result of changing the rate of limb joint extension before impact and/or changing the duration over which these movements occur. These possibilities suggest distinct motor strategies that vary in complexity to achieve the same result at impact.…”

“…Yet, previous examinations of anuran forelimb kinematics have not addressed this question, instead emphasizing important features of the landing event itself (Griep et al, 2013;Nauwelaerts and Aerts, 2006), the role of pectoral girdle anatomy (Emerson, 1983;Griep et al, 2013) or more general kinematics of the hop cycle (Peters et al, 1996). Recent work by Azizi and Abbott (2013) suggests that elbow excursions change with hop distance in B. marinus. During toad hopping, shortening and lengthening strains in the m. anconeus, a monoarticular elbow extensor, increase with hop length as the elbows extend before impact and flex after impact, respectively.…”

“…During toad hopping, shortening and lengthening strains in the m. anconeus, a monoarticular elbow extensor, increase with hop length as the elbows extend before impact and flex after impact, respectively. Azizi and Abbott (2013) argue that these changes in fascicle strain before and after impact likely parallel one another and are important for preventing injuries associated with overstretching muscles involved in dissipating energy during landing (Azizi and Abbott, 2013). While one can infer distance-dependent elbow excursions based on these patterns of fascicle length change, such excursions have not been measured directly.…”

“…Cane toads, Bufo marinus Linnaeus 1758, have recently received considerable attention as a model for studying the control of landing (Gillis et al, 2010;Akella and Gillis, 2011;Azizi and Abbott, 2013;Ekstrom and Gillis, 2015) because unlike more basal anurans, which often crash-land head or trunk first (Essner et al, 2010), cane toads routinely perform controlled, coordinated landings. To enable coordinated landing, they position their body and limbs appropriately in mid-air so as to align the ground reaction force vector close to the center of mass , allowing them to balance on their forelimbs momentarily as they lower their hindlimbs to the ground (Akella and Gillis, 2011;Gillis et al, 2010;Griep et al, 2013).…”

Role of axial muscles in powering mouth expansion during suction feeding in Largemouth Bass

“…Power is the product of force and velocity, so a muscle must generate both force and positive shortening velocity to produce power. Active muscles can produce force without changing length, such as limb muscles supporting the body (Roberts et al, 1997), or produce force while lengthening to absorb energy, as during the landing phase of a jump (Azizi and Abbott, 2013). However, the power required to explosively expand the mouth during suction feeding can only be produced by actively shortening muscles.…”