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

Abstract

Hollow cylindrical muscular organs are widespread in animals and are effective in providing support for locomotion and movement, yet are subject to significant non-uniformities in circumferential muscle strain. During contraction of the mantle of squid, the circular muscle fibers along the inner (lumen) surface of the mantle experience circumferential strains 1.3 to 1.6 times greater than fibers along the outer surface of the mantle. This transmural gradient of strain may require the circular muscle fibers near the inner and outer surfaces of the mantle to operate in different regions of the length-tension curve during a given mantle contraction cycle. We tested the hypothesis that circular muscle contractile properties vary transmurally in the mantle of the Atlantic longfin squid, Doryteuthis pealeii. We found that both the length-twitch force and length-tetanic force relationships of the obliquely striated, central mitochondria-poor (CMP) circular muscle fibers varied with radial position in the mantle wall. CMP circular fibers near the inner surface of the mantle produced higher force relative to maximum isometric tetanic force, P0, at all points along the ascending limb of the length-tension curve than CMP circular fibers near the outer surface of the mantle. The mean ± s.d. maximum isometric tetanic stresses at L₀ (the preparation length that produced the maximum isometric tetanic force) of 212 ± 105 and 290 ± 166 kN m(-2) for the fibers from the outer and inner surfaces of the mantle, respectively, did not differ significantly (P=0.29). The mean twitch:tetanus ratios for the outer and inner preparations, 0.60 ± 0.085 and 0.58 ± 0.10, respectively, did not differ significantly (P=0.67). The circular fibers did not exhibit length-dependent changes in contraction kinetics when given a twitch stimulus. As the stimulation frequency increased, L₀ was approximately 1.06 times longer than LTW, the mean preparation length that yielded maximum isometric twitch force. Sonomicrometry experiments revealed that the CMP circular muscle fibers operated in vivo primarily along the ascending limb of the length-tension curve. The CMP fibers functioned routinely over muscle lengths at which force output ranged from only 85% to 40% of P₀, and during escape jets from 100% to 30% of P₀. Our work shows that the functional diversity of obliquely striated muscles is much greater than previously recognized.