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Review
. 2010 Jun;20(3):347-52.
doi: 10.1016/j.conb.2010.02.002. Epub 2010 Mar 2.

Multisensory systems integration for high-performance motor control in flies

Affiliations
Review

Multisensory systems integration for high-performance motor control in flies

Mark A Frye. Curr Opin Neurobiol. 2010 Jun.

Abstract

Engineered tracking systems 'fuse' data from disparate sensor platforms, such as radar and video, to synthesize information that is more reliable than any single input. The mammalian brain registers visual and auditory inputs to directionally localize an interesting environmental feature. For a fly, sensory perception is challenged by the extreme performance demands of high speed flight. Yet even a fruit fly can robustly track a fragmented odor plume through varying visual environments, outperforming any human engineered robot. Flies integrate disparate modalities, such as vision and olfaction, which are neither related by spatiotemporal spectra nor processed by registered neural tissue maps. Thus, the fly is motivating new conceptual frameworks for how low-level multisensory circuits and functional algorithms produce high-performance motor control.

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Figures

Figure 1
Figure 1
Behavioral features and multisensory systems. (A) A cartoon highlighting the central sensory-ecological challenges to a fly: (i) in the absence of sensory cues, search with short inter-saccade intervals (ISI), (ii) upon acquiring a sensory signal, track the unpredictable odor plume, (iii) visually stabilize heading and avoid collisions. (B) Select sensory inputs.
Figure 2
Figure 2
Visual-olfactory behavioral algorithms. (A) A fly tethered within an electronic visual flight simulator is presented with a plume of food odor. In response to oscillation of the visual panorama in an increasing frequency sweep, flies adjust their wing kinematics for a classical optomotor response. The difference in wing beat amplitude across the two wings (ΔWBA) is proportional to yaw torque. (B) A fly tethered to a pin and suspended in a magnetic field beats its wings and steers freely in the horizontal (yaw) plane. A plume of food odor is delivered at one side of the circular arena (0 degrees, orange triangle). At the start of the trial, the animal is positioned 90 degrees to the right of the plume (blue arrow). Solid lines indicate individual flight trajectories, grayscale coded for individuals. Silhouettes indicate approximate heading at three time points. The spatial odor gradient is not drawn to scale.
Figure 3
Figure 3
Gradient tracking requires antennae to be mechanically functional. Experiments are similar to those in Figure 2, except that the mechanosensory Johnston's organ (JO) of the left antenna was immobilized with non-toxic epoxy (indicated in red).
Figure 4
Figure 4
Multisensory reflex loops revealed by electrophysiology.

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