S- and C-start escape responses of the muskellunge (Esox masquinongy) require alternative neuromotor mechanisms

Abstract

The startle response is a model system for examining the neural basis of behavior because of its relatively simple neural circuit organization and kinematic pattern. In fishes, the two primary types of startle behavior differ in their initial movements. In the C-start type of startle, the fish bends into a C shape, while the S-start involves an S-shaped body bend. Although considerable research has focused on determining how the C-start is generated neurally, S-start neurobiology has not been examined. I quantify the kinematics and electromyographic patterns of the initial movements of the C-start and S-start behaviors of the muskellunge (Esox masquinongy) to test three hypotheses for how the S-start is generated. (i) The S-start is generated by the same motor neural circuit as the C-start, but passive bending of the tail causes the body to take on an S shape. (ii) The S-start is generated by the same motor neural circuit as undulatory swimming. (iii) The S-start is generated by an independent neural mechanism from that used either in the C-start or in undulatory swimming. Results from kinematics and muscle activity patterns support the third hypothesis. In the muskellunge, the S-start is a high-performance startle behavior with peak angular velocity and peak angular acceleration of its initial bending comparable with those of the C-start and higher than would be expected for undulatory swimming. The S-start motor pattern, however, is distinct from the C-start motor pattern in having simultaneous muscle activity anteriorly on one side of the body and posteriorly on the opposite side. In contrast, the C-start is characterized by simultaneous unilateral muscle activity along the full length of the body. Alternative models are proposed for S-start neural circuit organization involving reticulospinal and local control of muscle activity.