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Fast muscle in squid (Loligo pealei): contractile properties of a specialized muscle fibre type

William M. Kier¹ and Nancy A. Curtin²

¹ Department of Biology, CB 3280 Coker Hall, University of North Carolina, Chapel Hill, NC 27599-3280, USA
² Biological Structure and Function Section, Division of Biomedical Sciences, Faculty of Medicine, Fleming Building, Imperial College, London SW7 2AZ, UK

View larger version (88K): [in a new window]   Fig. 1. Schematic diagram of cross sections of the tentacular stalk (A) and arm (B) of the squid Loligo pealei. The core of the tentacle and the arm consists of a densely packed mass of transverse muscle fibres (T) oriented perpendicular to the long axis of the appendages. The axial nerve cord (Ax) and longitudinal muscles (L) are also visible in the diagram. The muscle fibre bundle preparations (shaded) were obtained by cutting a small section from a transverse slice of the arm or tentacle. The foil clips used to hold the preparation in the testing apparatus were attached to the ends of the preparation (shaded and cross-hatched) in such a way that only transverse muscle fibres were present between the clips.

View larger version (209K): [in a new window]   Fig. 2. Transmission electron micrographs of longitudinal sections of the transverse muscle fibres of the tentacle (A) and arm (B) of Loligo pealei. The extensive sarcoplasmic reticulum (SR) of the cross-striated tentacle fibres is visible. Note the short sarcomeres and short thick filaments of the tentacle fibres compared with the much longer thick filaments apparent in the obliquely striated arm fibres. Scale bar, 1 µm.

View larger version (17K): [in a new window]   Fig. 3. Twitch force (A) and length (B) of a muscle fibre bundle preparation from the transverse muscle mass of the tentacle of Loligo pealei. The recordings of twitch force and length are superimposed after a stimulus at time zero. The highest force recording was obtained during an isometric (constant-length) twitch, and the others (a, b, c, d) were obtained during isotonic twitch with the force clamped to four different levels. The vertical lines mark the point at which force was measured. The slopes of the dashed lines on the length recordings give the velocity of shortening, and the vertical lines are the same times at which force was measured and mark the centre of the section from which the slopes were measured.

View larger version (16K): [in a new window]   Fig. 4. Force/velocity relationship for a single tentacle transverse muscle bundle preparation (filled circles) and a single arm transverse muscle bundle preparation (open circles). Force is expressed relative to the isometric force of the preparation (mean of repeat twitches for the tentacle and repeat 100 ms, 50 Hz tetani for the arm). Velocity is expressed in L0 s-1, where L0 is the length of the preparation at which peak isometric force is produced. The lines were fitted to the data using Hill's single hyperbolic function (see text and Table 1, tentacle preparation 6 and arm preparation 6).

View larger version (15K): [in a new window]   Fig. 5. Summaries of the length/active force relationships for tentacle transverse muscle fibre bundle preparations (A) during twitch stimulation (N=10) and arm transverse muscle fibre bundle preparations (B) during tetanic stimulation for 100 ms at 50 Hz (filled circles, N=6) and twitch stimulation (open circles, N=5). Force is expressed relative to the preparation's peak force for the same pattern of stimulation, and length is expressed relative to that giving this peak force.

View larger version (19K): [in a new window]   Fig. 6. Length/force relationship of a single arm (A) and a single tentacle (B) transverse muscle fibre bundle preparation. Force is expressed relative to the peak force P0 during twitch stimulation, and the preparation length is expressed relative to the optimal length for active force production, L0. Filled circles represent the active force produced in response to twitch stimulation and open circles represent the passive force produced in the absence of stimulation.

View larger version (20K): [in a new window]   Fig. 7. Superimposed recordings of force produced in response to stimulation at frequencies of 1 (twitch), 5, 10, 20, 40, 80, 120 and 160 Hz for 0.2 s (indicated by the horizontal bar) for a tentacle transverse muscle fibre bundle preparation (A) and an arm transverse muscle fibre bundle preparation (B).

View larger version (14K): [in a new window]   Fig. 8. Pooled stimulus frequency/force relationship data for tentacle muscle fibre bundle preparations (filled circles, N=10) and arm muscle fibre bundle preparations (open circles, N=10). Force is expressed relative to the preparation's maximum observed force. Values are means ± S.D.