Head waving in Aplysia californica. II. Functional anatomy and muscular activity during behaviour.

Bending and twisting movements of the body during head-waving behaviour of the sea hare Aplysia californica are produced by the concerted action of the muscles of the body wall on the hydrostatic skeleton formed by the haemocoel and internal organs. In this study, we describe the orientations and possible mechanical actions of muscles in the body wall. We also describe the spatial and temporal patterns of longitudinal muscle activity during different head-waving movements in a freely moving animal. The body-wall muscles are arranged as a network of longitudinal, circular and left- and right-handed helical muscle fascicles. Each fascicle consists of a few to several hundred muscle fibres enclosed in a connective tissue sheath. The sheath also connects muscle fascicles of different orientations at the points where they cross, forming a tightly connected network. In addition, a series of large longitudinal muscle fascicles, including the lateral columellar muscles, lies against the inside wall of the dorsal hemicylinder of the animal. In animals with hydrostatic skeletons, longitudinal and circular muscles are necessary for producing all basic elongation, shortening and bending movements, and in Aplysia, the extensive distribution of helical muscles provides the animal with the ability to twist its body about the longitudinal axis, as is observed during horizontal head-waving movements. Muscle activity in the lateral muscles is antiphasically coordinated during horizontal bends, and when the animal is bent to one side, movement towards the centre is accompanied by muscle activity on the side of shortening, i.e. there is no passive return to centre. The muscles near the holdfast are the most active during head-waving movements, with relatively little activity in the head region. The activity of dorsal muscles corresponds to both the existing vertical posture of the body and to discrete dorsal bending movements. In most cases, depression of the head is passive, i.e. both dorsal and ventral longitudinal muscles relax, although foot muscles may also be involved. These observations, together with the constancy of the hydrostatic pressure in the haemocoel during all movements in animals attached to the substratum, suggest specific patterns of motor neurone coordination during different movements.