Translation of sensory input into behavioral output via an olfactory system

Abstract

We investigate the logic by which sensory input is translated into behavioral output. First we provide a functional analysis of the entire odor receptor repertoire of an olfactory system. We construct tuning curves for the 21 functional odor receptors of the Drosophila larva and show that they sharpen at lower odor doses. We construct a 21-dimensional odor space from the responses of the receptors and find that the distance between two odors correlates with the extent to which one odor masks the other. Mutational analysis shows that different receptors mediate the responses to different concentrations of an odorant. The summed response of the entire receptor repertoire correlates with the strength of the behavioral response. The activity of a small number of receptors is a surprisingly powerful predictor of behavior. Odors that inhibit more receptors are more likely to be repellents. Odor space is largely conserved between two dissimilar olfactory systems.

Figure 1. Odor responses

(A) Responses to odorants at a 10^-2 dilution. “.”, n<50 spikes/s; “+”, 50≤n<100 spikes/s; “++”, 100≤n<150 spikes/s; “+++”, 150≤n<200 spikes/s; “++++”, n≥200 spikes/s. “-” denotes inhibition to ≤50% of the spontaneous firing rate. Inhibition was not calculated for Or47a; its low spontaneous firing rate (<4 spikes/s) made it difficult to quantitate inhibition. Each value represents the mean activity during a 0.5 s odor stimulation period. Spontaneous activity and response to solvent alone have been subtracted from response values. Numerical values are provided in Table S1. n≥6. Responses of Or30a, Or42a, Or45, Or45a, Or49a, Or59a, Or67b, Or74, Or85c, Or94, and Or94b were taken from (Kreher et al., 2005). Odorants are color coded by functional group: pink=organic acid; light green=terpene; gray=aldehyde; yellow=ketone; light blue=aromatic; red=alcohol; dark green=ester. (B) Responses to odorants at a 10^-4 dilution. n≥6.

Figure 2. Tuning breadths of larval odorant receptors

(A) Tuning curves for odorants at a 10^-2 dilution. Odorants are arranged to give the smoothest curve, with order of odorants differently arranged for each receptor; odorants that elicit the strongest responses are near the center of the distribution, while odorants that elicit weak responses are near the edges. Negative values indicate inhibitory responses. The graphs are ordered according to the number of odorants that elicit responses >100 spikes/s. The first four graphs are ordered according to the strongest response of each receptor. (B) Tuning curves of receptors to odorants at a 10^-4 dilution.

Figure 3. Behavioral responses to odorants

(A) Olfactory behavioral assay. Left, initial conditions; right, response to the odor after five minutes. Odorant was loaded on left filter paper disk. Taken from Monte et al. (1989). (B) Behavioral responses to 10^-2 odorant dilutions. Each bar represents RI±SEM; n=10.

Figure 4. Odor space

(A) Three-dimensional projections of odor space based on Euclidean distances (left) and angular distances (right), constructed using Multi-Dimensional Scaling. Data are from odorants tested at 10^-2 dilutions. Odorants are color coded by functional group as in Figure 1. (B) Closest and most distant odorant pairs as measured in Euclidean distance. (C) Closest and most distant odorant pairs as measured in angular distance.

Figure 5. Behavioral responses to point source odors are reduced by the presence of masking odors

(A) Masking of a point source of ethyl acetate (diluted 10^-4) with dilutions of ethyl acetate. (B) Masking of a point source of ethyl acetate (10^-4) with other odorants. Masking of a point source of (C) 2-heptanone (10^-2); (D) 3-octanol (10^-2); (E) E2-hexenal (10^-2); (F) ethyl butyrate (10^-2); (G) 2,3-butanedione (10^-2). Each bar represents RI±SEM, n=6, except that in the case in which 2,3-butanedione was masked with propyl acetate, n=4.

Figure 6

Relationship between odor masking and angular distance in a 21-receptor odor space. A high masking index value indicates that fewer larvae were attracted to the point source odor in the presence of the masking odor than in the presence of the solvent alone.

Figure 7. The response to one odorant depends on two receptors

(A) Behavioral response of wild-type to ethyl acetate. For entire figure, error bars=SEM; n=10. (B) Electrophysiological responses to ethyl acetate conferred by Or42a and Or42b in the empty neuron system; n=6 (C) Behavioral responses of larvae with mutant alleles of Or42a or Or42b to ethyl acetate; 6≤n≤10. (D) Behavioral responses to 2-heptanone and propyl acetate, at 10^-2 dilutions; n=6. Responses are not statistically different from wild-type controls (p>0.05).

Figure 8

Comparison of observed behavior and behavior predicted by the model based on five receptors: Or42a, Or45a, Or74a, Or82a, and Or85c. RI values are logit transformed for statistical rigor.