A Multifunction Muscle in Squid

Abstract

Some striated muscles are multifunctional; they serve several different roles during locomotion and movement, including acting as motors, brakes, struts, or springs. The few multifunctional muscles that have been reported occur in the cross-striated muscles of animals with complex, jointed, skeletal support systems. In the comparatively simple muscular system of a cephalopod mollusc, we identified an obliquely striated muscle, the nuchal retractor muscle, which appears to be multifunctional. The nuchal retractor is composed of two different fiber types, mitochondria-rich (MR) and mitochondria-poor (MP) fibers; shortening of these fibers retracts the head toward the mantle. Synchronized measurements of head movement (as a proxy for nuchal retractor length) and muscle activation revealed that, while the MP nuchal retractor muscle fibers were activated only for head retractions that occurred during escape jet locomotion, the MR fibers were activated 1) as the head retracted during escape jets and a few jets used during slow swimming, 2) during brief periods of head stasis as the animal changed swimming direction, and 3) during the rapid head extensions that followed an escape jet. Our results suggest that the nuchal retractor muscle may function as a motor, a brake, and, occasionally, a strut. More broadly, our findings suggest that multifunctionality is not restricted to cross-striated fibers or to the muscles of animals with jointed skeletal support systems.