If firing phase determines the biomechanical properties of the steering muscles, and as a consequence the precise motion of the wings, what signals tell the muscles when to fire? Experiments in which sensory nerves were systematically ablated indicate that the firing phase of steering motor neurons is driven, not by a central pattern generator, but rather by mechanosensory afferents on the wing and haltere (Heide, 1983
). The wing is equipped with arrays of campaniform sensilla, strain-sensitive structures imbedded within the exoskeleton (Cole and Palka, 1982; Gnatzy et al., 1987). In blowflies, a subset of these sensors make strong monosynaptic connections with the motor neurons of steering muscles (Fayyazuddin and Dickinson, 1996). Stroke-by-stroke input from wing sensors is capable of entraining steering motor neurons, thus ensuring that muscles fire at particular phases within the cycle (Fayyazuddin and Dickinson, 1999).
Halteres are the tiny club-shaped hindwings characteristic of all flies. During flight, the halteres beat in precise anti-phase with the forewings, thereby activating several hundred specialized mechanosensory cells at the base of the structures. The sensory cells are organized into five external fields of campaniform sensilla and one internal chordotonal organ (Pringle, 1948). Most of the fields encode the back and forth motion of the haltere in stable flight, and thus may act as their homologues on the wing to provide important timing signals to lock the steering muscles into particular phases of the stroke cycle. However, one of the campaniform fields (dorsal field 2, dF2) appears unique in that it is not sensitive to the back and forth beating of the haltere, but instead encodes the deflection of the haltere perpendicular to its stroke plane. During flight, such deflections are caused by Coriolis forces (Pringle, 1948; Nalbach, 1993), which act on the rapidly beating halteres whenever the fly's body rotates. The Coriolis-sensitive cells of dF2 make mixed electrical/chemical synapses with the motor neurons of steering muscles (Fayyazuddin and Dickinson, 1996; Trimarchi and Murphey, 1997), which are strong enough to temporarily override the phasic input from the wing afferents (Fayyazuddin and Dickinson, 1999), thereby shifting the timing of muscle activation in each stroke (Fig. 3B). Such modulation in steering muscle activity presumably causes alterations in wing motion and aerodynamic forces.
The critical role of the haltere in flight stability was first identified in 1714 by William Derham, who showed that a fly could not remain airborne if its tiny halteres were surgically removed (Derham, 1714
). Recent experiments on animals tethered within rotating flight simulators indicate that animals exhibit robust compensatory changes in wing amplitude and frequency to imposed mechanical rotation (
Fig. 3C) (Nalbach and Hengstenberg, 1994
; Dickinson, 1999
). The sign of the reflexes are such that they would act to counter any imposed perturbations, bringing the animal back to a stable orientation.
The haltere-motor circuits that counteract imposed rotation are so rapid and robust that it raises the question of how such reflexes are over-ridden during voluntary maneuvers such as saccades. One possibility is that the nervous system can adjust the gain of haltere reflexes to inhibit them during voluntary behaviors. In the blowfly Calliphora, descending visual interneurons activate tiny steering muscles of the haltere. By altering the kinematics of haltere motion, these steering muscles might either increase or decrease the sensitivity of the Coriolis-sensitive sensilla (Chan et al., 1998). Alternatively, if this descending input to haltere steering muscles produces changes in the haltere stroke plane that mimic those produced by rotation of the body, then the system might function to initiate voluntary maneuvers by generating "virtual" flight perturbations. This would be analogous to steering an aircraft by fooling an autopilot into responding to a non-existing course deviation. A third possibility is that the haltere-mediated reflexes are always operational, but that descending commands perturb the system just long enough to result in a change in flight path.
One of the most critical tasks of flight control circuitry is to integrate local mechanosensory feedback from the wings and halteres with descending commands from the visual system, such as those that trigger saccades. This fusion of sensory feedback is complicated by the fact that the visual and olfactory systems transduce and process sensory information on a slow time scale compared to the mechanoreceptors on the wing and haltere (Heide, 1983). Because the raw output from the visual system is not phase-locked with wing motion, it is inappropriate as direct input to steering motor neurons. Somehow the nervous system must combine descending commands with phasic input from thoracic mechanoreceptors so that the visual circuits activate steering at biomechanically-appropriate phases of the stroke cycle. How flight circuits accomplish this critical splicing of descending commands with phasic feedback is not well understood. Descending commands, such as the expansion signals that trigger saccades, are conveyed by a set of descending interneurons that project to flight circuits in the thorax. Anatomical evidence in blowflies suggests that descending visual interneurons make direct connections with steering motor neurons (Strausfeld and Gronenberg, 1990). Thus, one possibility is that the splicing or chopping of descending information with thoracic feedback takes place via synaptic interactions directly on the dendrites of steering motor neurons. However, mechanoreceptors on the wing and halteres possess collateral projections that ascend to the subesophageal ganglion, where they could potentially converge on visual circuits upstream of the descending interneurons (Chan and Dickinson, 1996). Thus, it is also possible that the critical fusion takes place in the brain so that the descending commands are already phase-locked to the stroke cycle.
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