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Supercontracting muscle: producing tension over extreme muscle lengths

Anthony Herrel^1,*, Jay J. Meyers², Jean-Pierre Timmermans³ and Kiisa C. Nishikawa²

¹ Laboratory of Functional Morphology, Biology Department, University of Antwerp (UIA), Universiteitsplein 1, B-2610 Antwerp, Belgium
² Functional Morphology and Physiology Group, Biology Department, Northern Arizona University, PO Box 5640, Flagstaff, AZ 86001, USA
³ Laboratory of Cell Biology and Histology, Faculty of Medicine, University of Antwerp (RUCA), B-2020 Antwerp, Belgium

View larger version (20K): [in a new window]   Fig. 1. Schematic diagram illustrating the process of supercontraction. (A) Here, the muscle is completely extended, resulting in no overlap between thick and thin filaments. (B) Muscle in the contracted state, overlap between thick and thin filaments is optimal. (C) Muscle in an even further contracted state; thin filaments overlap and thick filaments abut on the Z-disk. In normal vertebrate cross-striated muscle, no force can be generated at this stage. (D) Muscle in supercontraction. The thick filaments have passed through the holes in the Z-disks and are starting to engage in bonding with the thin filaments of the adjacent sarcomere. (E) Muscle in complete supercontraction. After this stage, the thick filaments will physically interact with each other and the muscle can no longer generate force. The green bars represent the thick filaments, the blue bars the thin filaments and the red bars the elements of the Z-disk. In the sarcomere, polarities are such that the dark green part of the thick filament can engage in binding with the dark blue thin filament and the light green part of the thick filament with the light blue thin filament. Hypothetical cross-bridges formed between filaments of adjacent sarcomeres (in black) are indicated in D and E. Modified after Osborne (1967) and Hardie (1976).

View larger version (17K): [in a new window]   Fig. 2. Length/tension diagram for the m. hyoglossus of an adult Pogona vitticeps. In these experiments, the tongue of the lizard was attached to a force lever, its length was changed, the muscle was tetanically stimulated and the forces were recorded. The length/tension diagram for P. vitticeps is similar to that reported for other animals with typical cross-striated muscle, showing a rapid increase in tension, a distinct optimal length for contraction and a decrease in tension if the muscle is extended beyond its optimal length.

View larger version (106K): [in a new window]   Fig. 3. Transmission electron micrograph (longitudinal section) through the tongue retractor muscle (m. hyoglossus) of an adult Pogona vitticeps. (A) Muscle in the resting condition. Note how the thin filaments almost abut in the middle of the A-band. The Z-disk is of the normal continuous type typical of vertebrate cross-striated muscle. (B) Section through a muscle in the extended condition (140% of whole muscle resting length). Note how the sarcomeres are extended to only approximately 120% of their resting length. Even in the extended condition, the overlap between thick and thin filaments is large, allowing the muscle to generate near-maximal tension. Scale bar, 1 µm.

View larger version (109K): [in a new window]   Fig. 4. Transmission electron micrograph (longitudinal section) through the tongue retractor muscle (m. hyoglossus) of an adult Chameleo calyptratus. Note the perforations in the Z-disks (arrow) characteristic of supercontracting muscle. Scale bar, 1 µm.

View larger version (13K): [in a new window]   Fig. 5. Summary diagram illustrating the differences in contractile properties between a variety of muscles. Relative tension is plotted against optimal muscle length. The length/tension properties of a typical vertebrate cross-striated muscle are indicated in red (data for the tongue retractor in Pogona vitticeps). The length/tension diagram for the obliquely striated mantle muscle in Sepia officinalis is depicted in blue (Milligan et al., 1997). The length/tension properties of chameleon (Chameleo oustaleti) tongue retractor muscle are depicted in green (Herrel et al., 2001) and the length/tension properties for the body wall muscle of Calliphora erythrocephala (Hardie, 1976) are depicted in black. Both the chameleon and the Calliphora erythrocephala muscles are of the supercontracting type and are able to generate tension over extreme muscle lengths. Cuttlefish obliquely striated muscle (blue) seems to have intermediate length/tension properties and is able to generate tension over a wider range of muscle lengths than typical vertebrate cross-striated muscles (red).