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Odor-induced Oscillatory Activity in Drosophila CNS.

In mammals and the fruit fly, the vast array of odors in the environment is discriminated by a large number of receptor molecules [1, 2, 3]. Individual olfactory sensory neurons express only one of the many receptor genes [1, 2, 3]. Neurons expressing the same receptor gene project to the same glomerulus [4, 5, 6], providing the anatomical evidence for a spatial coding mechanism. Electrophysiological recordings from olfactory neurons suggest that the temporal pattern of their responses can also convey information about odor quality [7]. Odor-induced oscillatory activity, an indication of synchrony, has been observed in phylogenetically different species, including molluscs, insects, and mammals [7, 8, 9, 10, 11, 12].

The adult Drosophila antennal lobe, organized in spheroidal subcompartments termed glomeruli, receives about 1200 olfactory afferents from the antenna and 120 afferent fibers from the maxillary palp [13]. Although the fly and mammals share the similarity that receptor neurons expressing the same receptor gene project to one or two glomeruli in a stereotypic manner [4, 5, 6], there are only 60 receptor genes and 43 glomeruli in Drosophila, in contrast to the 1000 receptor genes and 1800 glomeruli within the olfactory bulb of mammals [1, 2, 3]. The lower complexity in anatomy and the rich behavioral repertoire in Drosophila makes it an attractive system with which to study olfaction. Moreover, sophisticated genetic tools and behavioral mutants can now also be used to study the olfactory system in Drosophila. Nevertheless, understanding mechanisms of odor discrimination in the CNS of the fly has been difficult due to a lack of physiological tools for functional studies.

Odor-induced oscillations have been observed in several insect species, including the locust, cockroach, honeybee, bumblebee, and wasp [7]. Local field potential LFP recordings show odor-induced oscillation at [sim]10 Hz which typically lasts for the duration of odor stimulation. I have investigated this phenomenon in the Drosophila CNS. LFPs were recorded with glass electrodes (tip, 5 [micro]m) that were filled with Drosophila HL3 saline and positioned with a motorized manipulator (MP285, Sutter). A patch clamp amplifier (EPC 7, Heka) was used, and the signal was filtered (band pass at 0.1 to 20 Hz) with a signal conditioner (CyberAmp, Axon Instruments) and recorded with software (AxoScope, Axon Instruments) run on a PC. Adult flies (less than a week after eclosion) were lightly anesthetized with [CO.sub.2] and decapitated. The heads were immobilized with wax on a microscope slide with the antennae pointing upward. A small opening was made on the dorsal cuticle for the extracellular recording.

Figure 1 shows LFP recordings from the CNS of the Canton-S wild-type fly that reveal an odor-induced oscillation. This phenomenon was confirmed in 6 preparations. A power spectrum analysis indicates that the major frequency components are less than 4 Hz (Fig. 1). This LFP oscillation signal appears to be sensitive to the position of the electrode, and the coordinates taken from the manipulator suggest that the recordings may have originated in the antennal lobe. Future experiments with GFP-labeled antennal lobe may help in identifying the sources of the oscillatory activity. The patterns of oscillation in response to the same odor appear to be roughly similar in sequential recordings from the same animal. The LFP patterns generated in response to peppermint (from McCormick) and amyl acetate (from Sigma) were distinguishable by eye. Moreover, the power spectrum analysis indicates that peppermint generates slightly more high frequency components.

This is the first LFP recording from the Drosophila CNS. The preliminary results presented here show that odor-induced oscillation occurs in Drosophila; this finding suggests that a temporal coding mechanism may be employed by the fly, and that the power of genetics may be applied in the future to decipher the physiological significance of the odor-induced oscillation.

I would like to thank Alan Gelperin for his generous support, Leonardo Belluscio for critical comments on the manuscript, and Carl Zeiss, Inc., and Axon Instruments, Inc., for providing equipment. This research was carried out in the Grass Laboratory at the Marine Biological Laboratory, Woods Hole, Massachusetts, and was supported by the Grass Foundation.

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Author:Wang, Jing W.
Publication:The Biological Bulletin
Geographic Code:1USA
Date:Oct 1, 2000
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