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mm 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mm 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mm 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 V max (2.15 ±0.26L 0 s -1 , where L 0 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

The mechanical properties of the mantle muscle of European cuttlefish (Sepia officinalis)

“…The mean shortening velocity of cuttlefish mantle muscle (3–3.2 L s −1 ) is similar to that of the European common squid ( A. subulata ; Milligan et al, 1997 ). The maximum shortening velocity in the functionally related obliquely striated funnel muscle of longfin squid is similar (2.2 L s −1 ; Rosenbluth et al, 2010 ) to that in adult cuttlefish (3 L s −1 ; this study). The mechanical function of these muscles is rather different: the funnel muscles play a key role in jet ejection, adjusting aperture size and amending the direction in which a jet will be ejected, while the mantle muscles power jet propulsion.…”

The length-force behavior and operating length range of squid muscle varies as a function of position in the mantle wall

“…For example, the tentacles of D. pealeii are elongated by 80% or more during prey capture (Kier, 1982) and then shorten to bring the prey within grasp of the arms, thereby requiring the obliquely striated longitudinal muscle fibers (Kier, 1985) that retract the tentacles to operate over a wide range of muscle lengths. In contrast, the obliquely striated funnel retractor muscle in the same animal experiences only small changes in length (±5%) during jetting, and operates nearly isometrically during the exhalant phase of the jet (Rosenbluth et al, 2010). In addition, the obliquely striated transverse muscle fibers of the arms of two squid species (D. pealeii and Sepioteuthis sepioidea) experience virtually no change in length while providing support for bending movements (Kier, 1982).…”

Functional Histology: The Tissues of Common Coleoid Cephalopods

“…Fibers bear a single elongated nucleus. Ultrastructural and functional descriptions of the organization of these fibers including the oblique organization of contractile filaments, dense bodies and sarcoplasmic reticulum can be found in Budelmann et al (1997) and Rosenbluth et al (2010). These fibers form the basis of the body muscles, which are most often observed in bands or bundles of parallel fibers with different orientations (see below).…”