Dataset Information

In vivo force-length and activation dynamics of two distal rat hindlimb muscles in relation to gait and grade.

ABSTRACT: Muscle function changes to meet the varying mechanical demands of locomotion across different gait and grade conditions. A muscle's work output is determined by time-varying patterns of neuromuscular activation, muscle force and muscle length change, but how these patterns change under different conditions in small animals is not well defined. Here, we report the first integrated in vivo force-length and activation patterns in rats, a commonly used small animal model, to evaluate the dynamics of two distal hindlimb muscles (medial gastrocnemius and plantaris) across a range of gait (walk, trot and gallop) and grade (level and incline) conditions. We use these data to explore how the pattern of force production, muscle activation and muscle length changes across conditions in a small quadrupedal mammal. As hypothesized, we found that the rat muscles show limited fascicle strains during active force generation in stance across gaits and grades, indicating that these distal rat muscles generate force economically but perform little work, similar to patterns observed in larger animals during level locomotion. Additionally, given differences in fiber type composition and variation in motor unit recruitment across the gait and grade conditions examined here for these muscles, the in vivo force-length behavior and neuromuscular activation data reported here can be used to validate improved two-element Hill-type muscle models.

SUBMITTER: Eng CM

PROVIDER: S-EPMC6955210 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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<i>In vivo</i> force-length and activation dynamics of two distal rat hindlimb muscles in relation to gait and grade.

Eng Carolyn M CM Konow Nicolai N Tijs Chris C Holt Natalie C NC Biewener Andrew A AA

The Journal of experimental biology 20191218 Pt 24

Muscle function changes to meet the varying mechanical demands of locomotion across different gait and grade conditions. A muscle's work output is determined by time-varying patterns of neuromuscular activation, muscle force and muscle length change, but how these patterns change under different conditions in small animals is not well defined. Here, we report the first integrated <i>in vivo</i> force-length and activation patterns in rats, a commonly used small animal model, to evaluate the dyna ...[more]

PMID: 31753907

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Project description:BackgroundKnowledge of the muscle's lengths at which maximum active isometric force is attained is important for predicting forces during movement. However, there is limited information about the in vivo force-length properties of a human muscle that plays crucial roles during locomotion; the tibialis anterior (TA). We therefore aimed to estimate TA's force-length relation from dorsiflexor torque-angle curves constructed from eight women and eight men.MethodsParticipants performed maximal voluntary fixed-end contractions with their right ankle dorsiflexors from 0° to 30° plantar flexion. Muscle fascicle lengths were estimated from B-mode ultrasound images, and net ankle joint torques were measured using dynamometry. Fascicle forces were estimated by dividing maximal active torques by literature-derived, angle-specific tendon moment arm lengths while assuming a fixed 50% force contribution of TA to the total dorsiflexor force and accounting for fascicle angles.ResultsMaximal active torques were higher at 15° than 20° and 30° plantar flexion (2.4-6.4 Nm, p ≤ 0.012), whereas maximal active TA fascicle forces were higher at 15° than 0°, 20° and 30° plantar flexion (25-61 N, p ≤ 0.042), but not different between 15° and 10° plantar flexion (15 N, p = 0.277). TA fascicle shortening magnitudes during fixed-end contractions were larger at 15° than 30° plantar flexion (3.9 mm, p = 0.012), but less at 15° than 0° plantar flexion (-2.4 mm, p = 0.001), with no significant differences (≤0.7 mm, p = 0.871) between TA's superficial and deep muscle compartments. Series elastic element stiffness was lowest and highest at lengths 5% shorter and 5% longer than optimum fascicle length, respectively (-30 and 15 N/mm, p ≤ 0.003).DiscussionTA produced its maximum active force at 10-15° plantar flexion, and its normalized force-length relation had ascending and descending limbs that agreed with a simple scaled sarcomere model when active fascicle lengths from within TA's superficial or deep muscle compartment were considered. These findings can be used to inform the properties of the contractile and series elastic elements of Hill-type muscle models.

Project description: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 (SM) in the American Toad (Bufo americanus) during hopping and within the sternohyoid (SH) muscle in the rat (Rattus rattus) during swallowing, and of spatially separated fascicles within the medial gastrocnemius (MG) muscle in the rat during trotting, we measured their corresponding in vitro (toad) or in situ (rat) force-length relationships (FLRs). For all three muscles, in vivo strain heterogeneity lasted for about 36-57% of the behavior cycle, during which one segment or fascicle shortened while the other segment or fascicle simultaneously lengthened. In the toad SM, the proximal segment shortened from the descending limb across the plateau of its FLR 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 SH muscle, the proximal segment tended to shorten on its ascending limb from 0.90 to 0.85 Lo while the distal segment tended to lengthen across Lo (0.96-1.12 Lo). In the rat MG 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 Lo. 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 FLRs 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 FLR in one muscle region does not necessarily represent other regions within the same muscle.

Project description:Stimulation of the mouse hindlimb via the sciatic nerve was performed for a 4-h period to investigate acute muscle gene activation in a model of muscle phenotype conversion. Initial force production (1.6 +/- 0.1 g/g body wt) declined 45% within 10 min and was maintained for the remainder of the experiment. Force returned to initial levels upon study completion. An immediate-early growth response was present in the extensor digitorum longus (EDL) muscle (FOS, JUN, activating transcription factor 3, and musculoaponeurotic fibrosarcoma oncogene) with a similar but attenuated pattern in the soleus muscle. Transcript profiles showed decreased fast fiber-specific mRNA (myosin heavy chains 2A and 2B, fast troponins T(3) and I, alpha-tropomyosin, muscle creatine kinase, and parvalbumin) and increased slow transcripts (myosin heavy chain-1beta/slow, troponin C slow, and tropomyosin 3y) in the EDL versus soleus muscles. Histological analysis of the EDL revealed glycogen depletion without inflammatory cell infiltration in stimulated versus control muscles, whereas ultrastructural analysis showed no evidence of myofiber damage after stimulation. Multiple fiber type-specific transcription factors (tea domain family member 1, nuclear factor of activated T cells 1, peroxisome proliferator-activated receptor-gamma coactivator-1alpha and -beta, circadian locomotor output cycles kaput, and hypoxia-inducible factor-1alpha) increased in the EDL along with transcription factors characteristic of embryogenesis (Kruppel-like factor 4; SRY box containing 17; transcription factor 15; PBX/knotted 1 homeobox 1; and embryonic lethal, abnormal vision). No established in vivo satellite cell markers or genes activated in our parallel experiments of satellite cell proliferation in vitro (cyclins A(2), B(2), C, and E(1) and MyoD) were differentially increased in the stimulated muscles. These results indicated that the molecular onset of fast to slow phenotype conversion occurred in the EDL within 4 h of stimulation without injury or satellite cell recruitment. This conversion was associated with the expression of phenotype-specific transcription factors from resident fiber myonuclei, including the activation of nascent developmental transcriptional programs.

Dataset Information

In vivo force-length and activation dynamics of two distal rat hindlimb muscles in relation to gait and grade.

Publications

<i>In vivo</i> force-length and activation dynamics of two distal rat hindlimb muscles in relation to gait and grade.

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