Sensory Basis and Functional Role of Eye Movements Elicited During Locomotion in the Land Crab Cardisoma Guanhumi

Abstract

Eye movements in the horizontal plane and the rotatory component of body movement have been continuously recorded in land crabs, Cardisoma guanhumi Latreille, walking freely in an arena. The results show that the eyes compensate for locomotor turns by moving in the opposite direction to the body, thus reducing the image motion of surrounding objects on the retina. Gains often approach unity, so that stabilization of the rotatory component of self-generated image motion is good. Of the three compensatory eye reflexes that could contribute to these responses, optokinetic responses play a major role, since the gain of the responses of freely walking blinded crabs was about half that of crabs that could see. Since blinded crabs held above a ball moved their eyes whenever they rotated the ball about a vertical axis (i.e. turned), a significant role for leg proprioceptor-driven eye movements is also presumed. It is unclear whether vestibular nystagmus, driven by the statocysts, also has a role to play. In contrast to the high-gain compensatory responses that accompany turns, the translatory component of locomotion elicits compensatory eye movements only under the most favourable circumstances, when the crab walks along a runway facing a set of stripes. Even then, the responses are of very low gain (0.02-0.09). Amongst several possible factors, this is partly because lateral ommatidia, which drive the optokinetic responses, will face the poles of the flow field during sideways walking, and partly because stationary contrasts (as occur at the poles of the flow field) reduce the gain of optokinetic responses. It is argued that, by compensating for turns but not translatory locomotor movements, crabs effectively separate the rotatory from the translatory components of the visual flow field around them. Since only the former can be used in course control, while only the latter provides information on ground speed and the three-dimensional layout of the environment, such a separation makes good functional sense.