A pinboard by
Alexandra M. Yarger

PhD Candidate, Case Western Reserve University


Bio-inspired drone technology requires a model system to emulate. What better system than flies?

Bio-inspired technology requires first and foremost an understanding of how the natural system behaves. What better model exists to base drone technology on than a fly?

Flies are able to perform complex acrobatic maneuvers because they possess specialized sensory organs called halteres. The flies' halteres are modified hind-wings that are used to detect body rotations during flight. Sensory information detected by halteres is rapidly transmitted to both the wings and the neck. This allows the fly to precisely and directly control the position of their head and body in space.

How is the nervous system of a fly able to function so quickly and precisely? How do flies differentiate between external forces (e.g. a gust of wind) and self-generated movement (e.g. actively turning)? My research investigates these questions and begins to unravel how flies are able to encode such rapid and diverse types of motions in 3 dimensions.


Haltere-mediated equilibrium reflexes of the fruit fly, Drosophila melanogaster.

Abstract: Flies display a sophisticated suite of aerial behaviours that require rapid sensory-motor processing. Like all insects, flight control in flies is mediated in part by motion-sensitive visual interneurons that project to steering motor circuitry within the thorax. Flies, however, possess a unique flight control equilibrium sense that is encoded by mechanoreceptors at the base of the halteres, small dumb-bell-shaped organs derived through evolutionary transformation of the hind wings. To study the input of the haltere system onto the flight control system, I constructed a mechanically oscillating flight arena consisting of a cylindrical array of light-emitting diodes that generated the moving image of a 30 degrees vertical stripe. The arena provided closed-loop visual feedback to elicit fixation behaviour, an orientation response in which flies maintain the position of the stripe in the front portion of their visual field by actively adjusting their wing kinematics. While flies orientate towards the stripe, the entire arena was swung back and forth while an optoelectronic device recorded the compensatory changes in wing stroke amplitude and frequency. In order to reduce the background changes in stroke kinematics resulting from the animal's closed-loop visual fixation behaviour, the responses to eight identical mechanical rotations were averaged in each trial. The results indicate that flies possess a robust equilibrium reflex in which angular rotations of the body elicit compensatory changes in both the amplitude and stroke frequency of the wings. The results of uni- and bilateral ablation experiments demonstrate that the halteres are required for these stability reflexes. The results also confirm that halteres encode angular velocity of the body by detecting the Coriolis forces that result from the linear motion of the haltere within the rotating frame of reference of the fly's thorax. By rotating the flight arena at different orientations, it was possible to construct a complete directional tuning map of the haltere-mediated reflexes. The directional tuning of the reflex is quite linear such that the kinematic responses vary as simple trigonometric functions of stimulus orientation. The reflexes function primarily to stabilize pitch and yaw within the horizontal plane.

Pub.: 26 Jun '99, Pinned: 13 Sep '17

Position-specific central projections of mechanosensory neurons on the haltere of the blow fly, Calliphora vicina.

Abstract: The halteres of Dipteran insects play an important role in flight control. They are complex mechanosensory devices equipped with approximately 400 campaniform sensilla, cuticular strain gauges, which are organized into five fields at the base of each haltere. Despite the important role of these mechanosensory structures in flight, the central organization of the sensory afferents originating from the different field campaniforms has not been determined. We show here that in the blow fly, Calliphora vicina, sensory afferents from the campaniform fields project to the thorax in a region-specific manner. Afferents from different fields have different projection profiles and in addition, the projection pattern of afferents from different regions of the same field may show further variation. However, central target regions of these afferents are not exclusive to particular sensory fields because cells from different fields can possess similar projection profiles. Convergence of afferent projections is not limited to axons from the haltere fields, but is also observed between afferents originating from the haltere fields and those from serially homologous fields on the radial vein of the wing. Although we have not determined the specific cellular targets of the haltere sensory cells, the afferents of a dorsal field could make potential contact with at least one identified wing steering motoneuron that is known to be important in turning maneuvers. Our results, thus, provide the anatomical basis for studying how mechanosensory information encoded by the complex fields on the base of the haltere is mapped onto different functional regions within the CNS.

Pub.: 03 Jun '96, Pinned: 13 Sep '17

A Descending Neuron Correlated with the Rapid Steering Maneuvers of Flying Drosophila.

Abstract: To navigate through the world, animals must stabilize their path against disturbances and change direction to avoid obstacles and to search for resources [1, 2]. Locomotion is thus guided by sensory cues but also depends on intrinsic processes, such as motivation and physiological state. Flies, for example, turn with the direction of large-field rotatory motion, an optomotor reflex that is thought to help them fly straight [3-5]. Occasionally, however, they execute fast turns, called body saccades, either spontaneously or in response to patterns of visual motion such as expansion [6-8]. These turns can be measured in tethered flying Drosophila [3, 4, 9], which facilitates the study of underlying neural mechanisms. Whereas there is evidence for an efference copy input to visual interneurons during saccades [10], the circuits that control spontaneous and visually elicited saccades are not well known. Using two-photon calcium imaging and electrophysiological recordings in tethered flying Drosophila, we have identified a descending neuron whose activity is correlated with both spontaneous and visually elicited turns during tethered flight. The cell's activity in open- and closed-loop experiments suggests that it does not underlie slower compensatory responses to horizontal motion but rather controls rapid changes in flight path. The activity of this neuron can explain some of the behavioral variability observed in response to visual motion and appears sufficient for eliciting turns when artificially activated. This work provides an entry point into studying the circuits underlying the control of rapid steering maneuvers in the fly brain.

Pub.: 11 Apr '17, Pinned: 13 Sep '17

The halteres of the blowfly Calliphora

Abstract: We quantitatively analysed compensatory head reactions of flies to imposed body rotations in yaw, pitch and roll and characterized the haltere as a sense organ for maintaining equilibrium. During constant velocity rotation, the head first moves to compensate retinal slip and then attains a plateau excursion (Fig. 3). Below 500°/s, initial head velocity as well as final excursion depend linearily on stimulus velocities for all three axes. Head saccades occur rarely and are synchronous to wing beat saccades (Fig. 5). They are interpreted as spontaneous actions superposed to the compensatory reaction and are thus not resetting movements like the fast phase of ‘vestibulo-ocular’ nystagmus in vertebrates. In addition to subjecting the flies to actual body rotations we developed a method to mimick rotational stimuli by subjecting the body of a flying fly to vibrations (1 to 200 μm, 130 to 150 Hz), which were coupled on line to the fly's haltere beat. The reactions to simulated Coriolis forces, mimicking a rotation with constant velocity, are qualitatively and to a large extent also quantitatively identical to the reactions to real rotations (Figs. 3, 7–9). Responses to roll- and pitch stimuli are co-axial. During yaw stimulation (halteres and visual) the head performs both a yaw and a roll reaction (Fig. 3e,f), thus reacting not co-axial. This is not due to mechanical constraints of the neck articulation, but rather it is interpreted as an ‘advance compensation’ of a banked body position during free flight yaw turns (Fig. 10).

Pub.: 01 Dec '94, Pinned: 31 Jul '17

A neural basis for gyroscopic force measurement in the halteres of Holorusia.

Abstract: Dipteran flight requires rapid acquisition of mechanosensory information provided by modified hindwings known as halteres. Halteres experience torques resulting from Coriolis forces that arise during body rotations. Although biomechanical and behavioral data indicate that halteres detect Coriolis forces, there are scant data regarding neural encoding of these or any other forces. Coriolis forces arise on the haltere as it oscillates in one plane while rotating in another, and occur at oscillation frequency and twice the oscillation frequency. Using single-fiber recordings of haltere primary afferent responses to mechanical stimuli, we show that spike rate increases linearly with stimulation frequency up to 150 Hz, much higher than twice the natural oscillation frequency of 40 Hz. Furthermore, spike-timing precision is extremely high throughout the frequency range tested. These characteristics indicate that afferents respond with high speed and high precision, neural features that are useful for detecting Coriolis forces. Additionally, we found that neurons respond preferentially to specific stimulus directions, with most responding more strongly to stimulation in the orthogonal plane. Directional sensitivity, coupled with precise, high-speed encoding, suggests that haltere afferents are capable of providing information about forces occurring at the haltere base, including Coriolis forces.

Pub.: 30 Aug '08, Pinned: 31 Jul '17

Biomechanical basis of wing and haltere coordination in flies.

Abstract: The spectacular success and diversification of insects rests critically on two major evolutionary adaptations. First, the evolution of flight, which enhanced the ability of insects to colonize novel ecological habitats, evade predators, or hunt prey; and second, the miniaturization of their body size, which profoundly influenced all aspects of their biology from development to behavior. However, miniaturization imposes steep demands on the flight system because smaller insects must flap their wings at higher frequencies to generate sufficient aerodynamic forces to stay aloft; it also poses challenges to the sensorimotor system because precise control of wing kinematics and body trajectories requires fast sensory feedback. These tradeoffs are best studied in Dipteran flies in which rapid mechanosensory feedback to wing motor system is provided by halteres, reduced hind wings that evolved into gyroscopic sensors. Halteres oscillate at the same frequency as and precisely antiphase to the wings; they detect body rotations during flight, thus providing feedback that is essential for controlling wing motion during aerial maneuvers. Although tight phase synchrony between halteres and wings is essential for providing proper timing cues, the mechanisms underlying this coordination are not well understood. Here, we identify specific mechanical linkages within the thorax that passively mediate both wing-wing and wing-haltere phase synchronization. We demonstrate that the wing hinge must possess a clutch system that enables flies to independently engage or disengage each wing from the mechanically linked thorax. In concert with a previously described gearbox located within the wing hinge, the clutch system enables independent control of each wing. These biomechanical features are essential for flight control in flies.

Pub.: 22 Jan '15, Pinned: 31 Jul '17