In Vivo and In Vitro Heterogeneity of Segment Length Changes in the Semimembranosus Muscle of the Toad

Abstract

Many studies examine sarcomere dynamics in single fibres or length–tension dynamics in whole muscles in vivo or in vitro, but few studies link the various levels of organisation. To relate data addressing in vitro muscle segment behaviour with in vivo whole muscle behaviour during locomotion, we measured in vivo strain patterns of muscle segments using three sonomicrometry crystals implanted along a fascicle of the semimembranosus muscle in the American toad (Bufo americanus; n= 6) during hopping. The centre crystal emitted an ultrasonic signal, while the outer crystals received the signal allowing the instantaneous measurement of lengths from two adjacent muscle segments. On the first day, we recorded from the central and distal segments. On the second day of recordings, the most distal crystal was moved to a proximal position to record from a proximal segment and the same central segment. When the toads hopped a distance of two body lengths, the proximal and central segments strained −15.1 ± 6.1 and −14.0 ± 4.9 % (i.e. shortening), respectively. Strain of the distal segment, however, was significantly lower and more variable in pattern, often lengthening before shortening during a hop. From rest length, the distal segment initially lengthened by 2.6 ± 2.0 % before shortening by 6.5 ± 3.2 % at the same hop distance. Under in vitro conditions, the central segment always shortened more than the distal segment, except when passively cycled, during which the segments strained similarly. When the whole muscle was cycled sinusoidally and stimulated phasically in vitro, the two adjacent segments strained in opposite directions over much (up to 34 %) of the cycle. These differences in strain amplitude and direction imply that two adjacent segments can not only produce and/or absorb varying amounts of mechanical energy, but can also operate on different regions of their force–length and force–velocity relationships when activated by the same neural signal. Understanding regional differences in contractile dynamics within muscles is therefore important to linking our understanding of sarcomere behaviour with whole muscle behaviour during locomotion.

Gradients of strain and strain rate in the hollow muscular organs of soft-bodied animals

“…It is often assumed that there are no regional differences in fibre strain within a striated muscle, though recent work on vertebrates has shown this assumption to be false (e.g. Huijing 1985;Pappas et al 2002;Ahn et al 2003;Higham et al 2008). Our finding that fibres at different locations within the same muscular organ experience very different strain and strain rates also contradicts this long-standing assumption.…”

Muscle performance during frog jumping: influence of elasticity on muscle operating lengths

“…Although the landing phase of a jump or a hop requires the absorption of energy, most frogs use their forelimbs and bodies rather than their hindlimbs for this function (Nauwelaerts & Aerts 2006). In fact, no EMG activity is observed in the hindlimb muscles of anurans during the landing phase of a jump or a hop (Olson & Marsh 1998;Ahn et al 2003). It is possible that the lack of eccentric loading allows frog hindlimb muscles to safely operate on the descending limb of the force-length curve with little threat of eccentric muscle damage.…”

Explosive Jumping: Extreme Morphological and Physiological Specializations of Australian Rocket Frogs (Litoria nasuta)

“…While the muscle mechanics measurements made in this study are unlikely to have exactly replicated the activation patterns and length changes used by rocket frogs during jumping, the size of rocket frogs would exclude usage of the techniques necessary to determine realistic length change waveforms. Previous sonomicrometry measurements during jumping in semimembranosus muscle of Bufo americanus (Ahn et al 2003) and plantaris longus muscle of jumping Rana catesbeiana combined with modeling of the frog plantaris longus muscle-tendon unit (Roberts and Marsh 2003) have demonstrated uncoupling of skeletal muscle length changes from whole-body movements during jumping. Rapid early shortening of plantaris longus muscle without movement of the frog causes stretching of tendons and consequent elastic energy storage, which subsequently enhances muscle power output during takeoff.…”