Roles of eyes, leg proprioceptors and statocysts in the compensatory eye movements of freely walking land crabs (Cardisoma guanhumi)

Abstract

The compound eyes, the canal organs of the statocysts and proprioceptors in the legs all generate compensatory eye movements in the horizontal plane in the land crab Cardisoma guanhumi. Frequency analyses of the compensatory eye reflexes elicited by each of these inputs show that visual (V) and proprioceptive (P) reflexes respond best below 0.1 Hz, while statocyst (S) reflexes only achieve a high gain above this frequency. They thus increase the range of frequencies over which compensation can occur. Eye and body movements were recorded in an arena under all possible combinations of crabs seeing or blind (V+ or V-), with or without statocysts (S+ or S-) and freely walking or passively transported on a trolley (P+ or P-). Intact crabs (V+S+P+) show good stabilisation of the eyes in space, the only movements with respect to external coordinates being saccadic resetting movements (fast phases of nystagmus). The eyes thus compensate well for body turns, but are unaffected by translatory movements of the body and turns that are not accompanied by a change in the orientation of the long axis of the body in space. In the absence of any one sense, compensation for rotation is significantly impaired, whether measured by the increase in the width of the histograms of changes in the angular positions of the eyes in space ( capdelta &phgr; E), by the mean angular velocity of the eyes (slope of regression line, mE) with respect to the angular velocity of the body (mB) or by response gain plotted against angular acceleration of body turn (a). The absence of two senses reduces the crab's ability to compensate still further, with the statocyst-only condition (V-S+P-) being little better than the condition when all three senses are absent (V-S-P-).Such multisensory control of eye compensation for body rotation is discussed both in terms of making use of every available cue for reducing retinal slip and in making available the information content of the optic flow field.