Compensatory head roll in the blowflyCalliphoraduring flight

Abstract

Video records were made of the blowfly Calliphora erythrocephala L. mainly during tethered flight in a wind-tunnel, to study its movements about the longitudinal body axis (roll). During undisturbed flight, flies hold their head on average aligned with the body but may turn it about all three body axes. Pitch and yaw turns of the head are comparatively small (20°), whereas roll turns can be large (90°), and fast (1200° s -1 ). When passively rolled, flies produce compensatory head movements during walking or flight; at rest this reflex is turned off. Flies perceive a static misalignment relative to the vertical, as well as roll motion up to 10000° s -1 . Within this range flies counteract an imposed roll with maximal gain at about 1000° s -1 . Compensatory head movements are made with very low latency (down to ∆t ≈ 5ms), and with considerable speed (up to ω = 1000° s -1 ). Flies may ‘disregard’ an apparent deviation from their correct orientation, and may superimpose spontaneous head movements on those elicited by a stimulus. Compensatory head movements generally undercompensate the imposed misalignment. Simultaneously, however, flies modify their wing pitch and wingbeat amplitude to produce a compensatory roll torque. Since head and body roll act simultaneously and in the same direction, the overall speed and degree of head realignment, relative to external coordinates, increase considerably. This is certainly an advantage for flight in turbulent air. In still air, without need to correct an imposed misalignment, flies nevertheless produce spontaneous fluctuations of their flight torque, and head roll movements in the opposite direction. This is to be expected if flies intend to keep their eyes aligned with the coordinates of the environment while spontaneously performing banked turns. The limits of fly vision and the advantages of compensatory head movements for different visually guided behaviour are discussed. Compensatory head roll movements give flies greater manoeuvrability when cruising than the visual system would allow, without such a stabilizing reflex.

Visual gaze control during peering flight manoeuvres in honeybees

“…The dorsal light response and gravity reception are potential mechanisms. In tethered flies, Hengstenberg et al (1986) found a very similar head roll response to a continuously rotating drum, with the difference that flies turned their head by +908, which is close to the mechanical limits of the fly's neck joint. In these experiments, however, the authors eliminated gravity and light gradients as an orienting vector for roll movements by mounting the fly vertically in a homogeneously illuminated striped drum.…”

Haltere Afferents Provide Direct, Electrotonic Input to a Steering Motor Neuron in the Blowfly,Calliphora

“…Although the haltere is subjected to inertial and gravitational forces, the sensory cells appear most sensitive to Coriolis forces acting on the end-knob during angular rotation of the body (Nalbach, 1993(Nalbach, , 1994. The compensatory reactions elicited by the halteres include head movements and changes in the wingstroke kinematics (Hengstenberg et al, 1986;Hengstenberg, 1988). The control of the wingstroke resides with a set of 17 small steering muscles that are typically active only during steering maneuvers .…”

Gaze control in the blowfly Calliphora: a multisensory, two-stage integration process

“…extrafoveal), they are seen less well than when correctly centered; familiar objects are less well recognized when seen in an unfamiliar orientation. [1][2][3] Thus, best visual perception requires upright stabilization of the eyes whereas high manoeuverability, as in a flying animal may require fast movements and oblique postures. This conflict of interest can be partly solved by mobile eyes which may be stabilized temporarily an the visual scene 5,6 and crustacea 7,8 but, until recently, very little in insects.…”