Behavioral context-dependent modulation of descending statocyst pathways during free walking, as revealed by optical telemetry in crayfish

Abstract

Crustacean posture control is based on a complex interaction between the statocyst input and other sensory inputs as well as the animal's behavioral context. We examined the effects of behavioral condition on the activity of descending statocyst pathways using an optical telemetry system that allowed underwater recording of neuronal signals from freely behaving crayfish. A functionally identified statocyst-driven interneuron that directionally responded to body tilting without a footboard and to tilting of the footboard was found to show complicated responses depending upon the ongoing behavior of the animal when it freely walked around in water on the aquarium floor. The spike firing frequency of the interneuron increased significantly during walking. When the animal stood or walked on the tilted floor, the interneuron activity represented the tilt angle and direction if the abdomen was actively flexed, but not if it was extended. Two other statocyst-driven descending interneurons were found to be affected differently by the animal's behavioral condition: the spike activity of one interneuron increased during walking, but its directional response on the tilted floor was completely absent during abdominal posture movements, whereas that of another interneuron was enhanced during abdominal extension only, representing the tilt angle and direction. The results obtained in this study provide the first experimental demonstration that crustacean postural control under natural conditions is dependent on very fine aspects of the animal's locomotor behavioral context, suggesting far more complex control mechanisms than those expected from the experimental data obtained in isolated and fixed animals.