Visual control of steering in locust flight: the effects of head movement on responses to roll stimuli

The contribution of head movement to the control of roll responses in flying locusts (Locusta migratoria) has been examined (i) on a flight balance, recording the angles through which the locust turns when following an artificial horizon; (ii) by recording activity in a pair of flight muscles in restrained conditions; and (iii) by observations on free flying locusts. Responses were compared when the head was free to turn about the thorax, as normal, and when the head was waxed to the thorax, blocking any relative motion between the two ('head-fixed'). These experiments suggest that the major signal generating corrective roll manoeuvres is the visual error between the angle of the head and the horizon, rather than a signal that includes a measure of the head-thorax angle. 1. On the flight balance in the head-free condition the roll angle of the thorax was consistently less than in the head-fixed state, and followed the stimulus with longer response lags. Furthermore, the difference between the angle of the thorax assumed during head-free and head-fixed rolls was close to the angle of the head relative to the thorax during head-free responses. 2. Records of activity of the forewing first basalar muscles (M97) were made during rotation of the horizon about immobilized animals. When the head could follow the horizon, the relative latency between activity in the left and right basalar muscles decreased as the head position turned to approach the displaced horizon. When head-fixed, the relative latency was directly proportional to horizon angle. 3. The relative latency between left and right M97 flight muscles correlates better with the visual error signal than with the horizon position signal, lagging by approximately 40 ms. 4. In the open air, head-fixed locusts appear able to fly as well as head-free locusts. These data suggest that the reduction in visual inputs caused by compensatory motion of the head during roll manoeuvres is not functionally replaced by inputs from cervical proprioceptors. Some reasons why the locust may nevertheless allow head movement relative to the thorax during flight are discussed.