Different segments within vertebrate muscles can operate on different regions of their force-length relationships

Abstract

To relate in vivo behavior of fascicle segments within a muscle to their in vitro force-length relationships, we examined the strain behavior of paired segments within each of three vertebrate muscles. After determining in vivo muscle activity patterns and length changes of in-series segments within the semimembranosus muscle in the American Toad (Bufo americanus) during hopping and within the sternohyoid muscle in the rat (Rattus rattus) during swallowing, and of spatially separated fascicles within the medial gastrocnemius muscle in the rat during trotting, we measured their corresponding in vitro (toad) or in situ (rat) force-length relationships. For all three muscles, in vivo strain heterogeneity lasted for about 36 to 57% of the behavior cycle, during which one segment or fascicle shortened while the other segment or fascicle simultaneously lengthened. In the toad semimembranosus muscle, the proximal segment shortened from the descending limb across the plateau of its force-length relationship from 1.12 to 0.91 of its optimal length (Lo), while the distal segment lengthened (by 0.04 ± 0.04 Lo) before shortening down the ascending limb from 0.94 to 0.83 Lo. In the rat sternohyoid muscle, the proximal segment tended to shorten on its ascending limb from 0.90 to 0.85 L₀ while the distal segment tended to lengthen across L₀ (0.96 to 1.12 L₀). In the rat medial gastrocnemius muscle, in vivo strains of proximal fascicles ranged from 0.72 to 1.02 Lo, while the distal fascicles ranged from 0.88 to 1.11 L₀. Even though the timing of muscle activation patterns were similar between segments, the heterogeneous strain patterns of fascicle segments measured in vivo coincided with different operating ranges across their force-length relationships simultaneously, implying differences in force-velocity behavior as well. The three vertebrate skeletal muscles represent a diversity of fiber architectures and functions and suggest that patterns of in vivo contractile strain and the operating range over the force-length relationship in one muscle region does not necessarily represent other regions within the same muscle.