The ability of an animal to detect, discriminate, and respond to odors depends on the functions of its olfactory receptor neurons (ORNs). The extent to which each ORN, upon activation, contributes to chemotaxis is not well understood. We hypothesized that strong activation of each ORN elicits a different behavioral response in the Drosophila melanogaster larva by differentially affecting the composition of its navigational behavior. To test this hypothesis, we exposed Drosophila larvae to specific odorants to analyze the effect of individual ORN activity on chemotaxis. We used two different behavioral paradigms to analyze the chemotaxis response of larvae to odorants. When tested with five different odorants that elicit strong physiological responses from single ORNs, larval behavioral responses toward each odorant differed in the strength of attraction as well as in the composition of discrete navigational elements such as runs and turns. Further, behavioral responses to odorants did not correlate with either the strength of odor gradients tested or the sensitivity of each ORN to its cognate odorant. Finally, we provide evidence that wild type larvae with all ORNs intact exhibit higher behavioral variance than mutant larvae that have only a single pair of functional ORNs. We conclude that individual ORNs contribute differently to the olfactory circuit that instructs chemotactic responses. Our results, along with recent studies from other groups, suggest that ORNs are functionally non-equivalent units. These results have implications for understanding peripheral odor coding.
Significance Statement: Olfactory behavior in the Drosophila larva is based on the activities of only 21 olfactory receptor neurons (ORNs). An intriguing question in the biology of sensory systems concerns the functional diversity among its ORNs. Through systematic olfactory behavior analyses we report that activation of each larval ORN differently influences discrete navigational elements such as runs and turns. One interpretation is that individual ORNs contribute differently to the olfactory circuit that leads to chemotactic response. This analysis of functional diversity among ORNs has implications for developing more reliable models of odor coding.
The authors declare no competing financial interests.
Funding sources: Research reported in this publication was supported by Startup Funds from the University of Nevada, Reno and by NIGMS of the National Institute of Health under grant number P20 GM103554.