The ultrastructure and contractile properties of a fast-acting, obliquely striated, myosin-regulated muscle: the funnel retractor of squids

Abstract

SUMMARYWe investigated the ultrastructure, contractile properties, and in vivo length changes of the fast-acting funnel retractor muscle of the long-finned squid Doryteuthis pealeii. This muscle is composed of obliquely striated, spindle-shaped fibers ~3 μm across that have an abundant sarcoplasmic reticulum, consisting primarily of membranous sacs that form ‘dyads’ along the surface of each cell. The contractile apparatus consists of ‘myofibrils’ ~0.25–0.5 μm wide in cross section arrayed around the periphery of each cell, surrounding a central core that contains the nucleus and large mitochondria. Thick myofilaments are ~25 nm in diameter and ~2.8 μm long. ‘Dense bodies’ are narrow, resembling Z lines, but are discontinuous and are not associated with the cytoskeletal fibrillar elements that are so prominent in slower obliquely striated muscles. The cells approximate each other closely with minimal intervening intercellular connective tissue. Our physiological experiments, conducted at 17°C, showed that the longitudinal muscle fibers of the funnel retractor were activated rapidly (8 ms latent period following stimulation) and generated force rapidly (peak twitch force occurred within 50 ms). The longitudinal fibers had low Vmax (2.15 ±0.26 L0 s−1, where L0 was the length that generated peak isometric force) but generated relatively high isometric stress (270±20 mN mm−2 physiological cross section). The fibers exhibited a moderate maximum power output (49.9 W kg−1), compared with vertebrate and arthropod cross striated fibers, at a V/Vmax of 0.33±0.044. During ventilation of the mantle cavity and locomotion, the funnel retractor muscle operated in vivo over a limited range of strains (+0.075 to −0.15 relative to resting length, LR) and at low strain rates (from 0.16 to 0.91 LR s−1 ), corresponding to a range of V/Vmax from 0.073 to 0.42. During the exhalant phase of the jet the range of strains was even narrower: maximum range less than ±0.04, with the muscle operating nearly isometrically during ventilation and slow, arms-first swimming. The limited length operating range of the funnel retractor muscles, especially during ventilation and slow jetting, suggests that they may act as muscular struts.