Mechanics of the fast-start: muscle function and the role of intramuscular pressure in the escape behavior of amia calva and polypterus palmas

Abstract

The fast-start escape response is a rapid, powerful body motion used to generate high accelerations of the body in virtually all fishes. Although the neurobiology and behavior of the fast-start are often studied, the patterns of muscle activity and muscle force production during escape are less well understood. We studied the fast-starts of two basal actinopterygian fishes (Amia calva and Polypterus palmas) to investigate the functional morphology of the fast-start and the role of intramuscular pressure (IMP) in escape behavior. Our goals were to determine whether IMP increases during fast starts, to look for associations between muscle activity and elevated IMP, and to determine the functional role of IMP in the mechanics of the escape response. We simultaneously recorded the kinematics, muscle activity patterns and IMP of four A. calva and three P. palmas during the escape response. Both species generated high IMPs of up to 90 kPa (nearly 1 atmosphere) above ambient during the fast-start. The two species showed similar pressure magnitudes but had significantly different motor patterns and escape performance. Stage 1 of the fast-start was generated by simultaneous contraction of locomotor muscle on both sides of the body, although electromyogram amplitudes on the contralateral (convex) side of the fish were significantly lower than on the ipsilateral (concave) side. Simultaneous recordings of IMP, escape motion and muscle activity suggest that pressure change is caused by the contraction and radial swelling of cone-shaped myomeres. We develop a model of IMP production that incorporates myomere geometry, the concept of constant-volume muscular hydrostats, the relationship between fiber angle and muscle force, and the forces that muscle fibers produce. The timing profile of pressure change, behavior and muscle action indicates that elevated muscle pressure is a mechanism of stiffening the body and functions in force transmission during the escape response.