BLOWFLY FLIGHT AND OPTIC FLOW II . HEAD MOVEMENTS DURING FLIGHT

performing fast and acrobatic flight manoeuvres. This flight behaviour must have important consequences for vision. First, fast turns can lead to motion blur, impairing vision of spatial details (Srinivasan and Bernard, 1975). Second, turns interrupt the pattern of optic flow that reveals the three-dimensional structure of the surroundings during translation (Koenderink, 1986). In principle, these adverse effects of flight behaviour can be alleviated by compensatory eye movements (Carpenter, 1988; Land, 1973, 1975; Steinman and Collewijn, 1980). For blowflies, with their compound eyes fixed to the head, these eye movements correspond to head movements. The head of blowflies has appreciable freedom of movement because the neck is flexible and controls head posture via an elaborate system of muscles (Strausfeld et al., 1987; Hengstenberg, 1992). Experiments on tethered flies show that head movements can indeed be used to partly compensate thorax rotations (roll, Hengstenberg et al., 1986; Hengstenberg, 1992; yaw, Land, 1973, 1975). In the studies of Land (1973, 1975), thorax rotations in the yaw direction (rotation around a vertical axis) occurred in fast steps (called thorax saccades). Between these saccades, the thorax and, in particular, the head were more stable. These experiments were subsequently challenged by Geiger and Poggio (1977), who argued that the saccadic behaviour was an artefact attributable to the appreciable mass and inertial momentum added to the animal by the tether. Using a lighter tether, they were unable to repeat the observations of Land (1973, 1975). Subsequent measurements on insects in free flight, however, have supported the existence of thorax saccades at least (Syritta pipiens, Collett, 1980; Musca domestica, Wagner, 1986). Unfortunately, using the techniques available (video and film), these experiments were unable to resolve head movements, gave little or no information on roll movements and had a rather low temporal resolution (typically 20 ms). With the development of a modified search coil technique suitable for measuring position and orientation in (almost) freely flying blowflies (Schilstra and van Hateren, 1998a,b, 1999), it has now become possible to re-address this question of how the head and thorax move during flight. The new technique was developed specifically to provide information about the spatiotemporal input received by the blowfly eye during normal flight: this input can be reconstructed from the stimuli on the walls of the flight cage and from the measured eye positions and orientations. The statistical properties of this input play an important role in recent theories of early visual processing (see van Hateren, 1992a,b). A full analysis of this input is beyond the scope of the present article, however. Instead, we will concentrate on the detailed properties of the head movements occurring during thorax saccades (see Schilstra and van Hateren, 1999). It is shown that the free-flight behaviour of blowflies can be separated into two sets of 1491 The Journal of Experimental Biology 202, 1491–1500 (1999) Printed in Great Britain © The Company of Biologists Limited 1999 JEB1990