A modified version of the unique cue theory accounts for olfactory compound processing in honeybees

Abstract

We investigated the capability of honeybees to discriminate between single odorants, binary olfactory mixtures, and ternary olfactory mixtures in olfactory conditioning of the proboscis extension reflex. In Experiment 1, three single odorants (A+, B+, and C+) and three binary mixtures of these odors (AB+, AC+, and BC+) were reinforced while the ternary compound, consisting of all three odors (ABC-), was nonreinforced. In Experiment 2, only one single odorant (A+) and one binary olfactory compound (BC+) were reinforced while the ternary compound (ABC-) consisting of the single odor and the binary compound was nonreinforced. We studied whether bees can solve these problems and whether the course of differentiation can be predicted by the unique cue theory, a modified unique cue theory, or Pearce's configural theory. Honeybees were not able to differentiate reinforced from nonreinforced stimuli in Experiment 1. However, summation to ABC observed at the beginning of training contradicts the predictions of Pearce's configural theory. In Experiment 2, differentiation between the single odorant A and the ternary compound developed more easily than between the binary compound BC and ABC. This pattern of differentiation is in line with a modified unique cue theory and Pearce's configural theory. Summation to ABC at the beginning of training, however, again was at odds with Pearce's configural theory. Thus, olfactory compound processing in honeybees can best be explained by a modified unique cue theory.

Figure 1

Conditioned proboscis extension response (% PER) along trials in an A+/B+/C+ and AB+/AC+/BC+ versus ABC- discrimination. The curve depicts the course of % PER to the reinforced single elements A+, B+, and C+ (•); the reinforced binary compounds AB+, AC+, and BC+ (▪); and the nonreinforced ternary compound ABC- (⋄) during acquisition along four blocks of training. For the single elements and the binary compounds, each block consists of the averaged response to all three elements or binary compounds on the given trial. For the ternary compound, each block consists of six sequential trials.

Figure 2

Conditioned proboscis extension response (% PER) along trials in an A+ and BC+ versus ABC- discrimination. The curve depicts the course of % PER to the reinforced single element A+ (•), the reinforced binary compound BC+ (▪), and the nonreinforced ternary compound ABC- (⋄) during acquisition along six blocks of training. For the single element and the binary compound, each block consists of one trial each, where as for the ternary compound, each block consist of two sequential trials.

Figure 3

Computer simulation of an A+ and BC+ versus ABC- discrimination including a contextual stimulus X of three different saliencies along 20 trials. The learning rate associated with the US (β) was 0.2 for reinforced trials and 0.1 for nonreinforced trials. The asymptotic level of associative strength (λ) was 100 for reinforced trials and 0 for nonreinforced trials. Each cycle contained one trial with A+, one trial with BC+, and two trials with ABC-. The salience of the context stimulus was varied from 0 to 3. The upper panel shows the discrimination task in which the context had a salience of 0 (as if no context was present at all). The middle panel shows the same discrimination task including a context with a salience of 1 (salience equal to that of the other CSs). The lower panel shows the discrimination task including a context with a salience three times higher than that of the other CSs. Initial summation to ABC- can be observed only under this condition.