Bilateral olfaction: two is better than one for navigation
© BioMed Central Ltd 2008
Published: 31 March 2008
Do animals require bilateral input to track odors? A recent study reveals that fruit fly larvae can localize odor sources using unilateral inputs from a single functional sensory neuron, but that an enhanced signal-to-noise ratio provided by dual inputs is helpful in more challenging environments.
Biological sensory systems often make use of asymmetries in sensory inputs to extract information about the environment. The visual system, for example, exploits disparities in the two-dimensional images obtained from the left and the right eyes to extract information about depth . The auditory system uses the phase and intensity differences of stereo inputs to localize sound sources . Relatively little is known about the importance of bilateral inputs in olfaction. Our own noses feature twin nostrils; insects have paired antennae. What advantages do such configurations provide? A recent study by Louis and colleagues  examined the significance of paired inputs for odor navigation in an animal offering numerous experimental advantages, the larva of the fruit fly, Drosophila melanogaster.
In the larva, the transduction of chemical stimuli into neural representations begins in two dorsally located olfactory organs that are about 100 micrometers apart. Each olfactory organ normally contains 21 sensory neurons, each expressing one or two receptor genes together with the universally coexpressed OR83b gene . Earlier studies by the authors had established that knocking out the OR83b co-receptor gene removes essentially all odor-driven behavior in these larvae . By randomly rescuing the co-receptor gene in either the left or the right olfactory organ in transgenic OR83b knockout preparations, the authors generated unilateral animals - perfect for answering interesting questions about bilateral chemoreception.
Is one just as good as two?
Do the larvae require a full complement of receptors to reliably locate odor sources? Surprisingly, transgenic larvae with unilateral input from a single olfactory neuron were able to locate odor sources just as well as wild-type larvae. In fact, bilateral transgenic larvae with a single functional receptor neuron in each of their olfactory organs actually showed greater odor sensitivity than wild-type larvae. This apparently odd result may point toward an odor-coding scheme in the wild type in which ensembles of sensors with a low signal-to-noise ratio are combined with inputs with a high signal-to-noise ratio. Or, alternatively, in the wild type, competition among downstream neurons driven by different receptor neurons could diminish overall sensitivity. Schemes like these may function to promote odor discrimination, another task mediated by the same circuitry.
The authors found that both transgenic and wild-type larvae navigate by constantly orienting themselves along the direction of the steepest local concentration gradient (Figure 1). The larval rate of turning was greatest in low-concentration regions and decreased as the larvae progressed towards the concentration peak. This 'direct chemotaxis' is strikingly different from the 'biased random walk' strategy used by bacteria, which change direction at random, but alter the intervals between turns to bias movement toward attractants and away from repellants .
Interestingly, the authors noticed a side-dependent bias in the unilateral animals. Both left- and right-sided animals have a single functional receptor neuron, yet right-sided larvae performed chemotaxis significantly better than their left-sided counterparts. In larvae (unlike in adult flies) sensory inputs from each side remain segregated throughout the peripheral olfactory pathway. Thus, the observed right-side bias suggests disparities in downstream processing. This inherent right-side bias is not unique to these larvae - lateralization of olfactory processing has also been reported in a few other invertebrate species . The importance of this bias for odor processing and olfactory behavior remains unclear.
The two olfactory organs are so close together in fruit fly larvae that any odor concentration differences between them would be undetectably slight, and so it seems unlikely that bilateral concentration comparisons could provide useful cues for successful navigation. So how do these organisms locate odor sources? The most likely possibility is that the larvae use a mechanism that allows comparisons between at least two consecutive concentration measurements made over time. Thus, the results from Louis et al.  suggest that a form of working memory of the concentration of recent samples is required for chemotaxis by Drosophila larvae.
Navigating complex environments
Adult flies may use a different strategy. Unlike larvae, in adults around 10-40 receptor neurons of the same type are present in each antenna and project bilaterally to both left and right antennal lobes. Hence, in the adult, integration of redundant inputs begins at a very early stage in olfactory processing. Whether this unique wiring scheme enhances the spatial comparison of simultaneous bilateral inputs  or only increases the number of redundant receptors and, therefore, the signal-to-noise ratio, remains unknown.
Stereo olfactory cues are more important for humans and other animals with olfactory organs that are well separated in space [8, 9]. Humans, for example, can track odors based on comparisons of concentration measurements made over time alone, but also use inter-nostril concentration differences to improve tracking performance: occluding one nostril or providing the same odor information to both nostrils significantly reduces a person's ability to locate odor sources quickly .
As shown by Louis and colleagues , Drosophila, with its simple brain structure and wealth of genetic tools, provides a useful system for the study of olfaction and odor-evoked behavior. It will be interesting to determine the role of bilateral inputs in adult flies and compare their navigation strategies with those of the larvae. And it will be especially interesting to explore the significance and neural basis of the transient, working memory processes apparently needed to mediate chemotaxis. The use of genetically manipulated flies and their larvae will no doubt contribute greatly to these efforts .
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