Generalization mediates sensitivity to complex odor features in the honeybee

Abstract

Animals use odors as signals for mate, kin, and food recognition, a strategy which appears ubiquitous and successful despite the high intrinsic variability of naturally-occurring odor quantities. Stimulus generalization, or the ability to decide that two objects, though readily distinguishable, are similar enough to afford the same consequence, could help animals adjust to variation in odor signals without losing sensitivity to key inter-stimulus differences. The present study was designed to investigate whether an animal's ability to generalize learned associations to novel odors can be influenced by the nature of the associated outcome. We use a classical conditioning paradigm for studying olfactory learning in honeybees to show that honeybees conditioned on either a fixed- or variable-proportion binary odor mixture generalize learned responses to novel proportions of the same mixture even when inter-odor differences are substantial. We also show that the resulting olfactory generalization gradients depend critically on both the nature of the stimulus-reward paradigm and the intrinsic variability of the conditioned stimulus. The reward dependency we observe must be cognitive rather than perceptual in nature, and we argue that outcome-dependent generalization is necessary for maintaining sensitivity to inter-odor differences in complex olfactory scenes.

Figure 1. Honeybees' responses to the test odors depended upon conditioning paradigm.

The filled circles represent the mean response probabilities to the test odors; the error bars indicate the standard errors predicted by a binomial response distribution. The control condition (black circles) represented a situation where honeybees received conditioning with one odor (the Δp_h = 0.0) in association with sucrose reward (N = 60). The red line represents the (+ +) condition in which a honeybee was conditioned with two odors (Δp_h = 0.0 and Δp_h = 0.2) both in association with sucrose reward (N = 98). The green line represents the (+ −) condition in which a honeybee was conditioned with the same two odors, but Δp_h = 0.0 was associated with sucrose and Δp_h = 0.2 was associated with salt punishment (N = 69).

Figure 2. Generalization gradients for honeybees as predicted from the logistic regression models fit to the data from Figure 1.

Generalization gradients for the honeybee and their relative discrimination thresholds were generated by evaluating the models fitted by the logistic regressions and extrapolating them over a wider range of Δp_h values than could be used in the experiments. The dotted lines show d′ thresholds (see Methods) calculated for the three conditions using signal-detection theory; the horizontal bars visible at the extrema show standard deviations on these thresholds.