Configural olfactory learning in honeybees: negative and positive patterning discrimination

Abstract

In an appetitive context, honeybees (Apis mellifera) learn to associate odors with a reward of sucrose solution. If an odor is presented immediately before the sucrose, an elemental association is formed that enables the odor to release the proboscis extension response (PER). Olfactory conditioning of PER was used to study whether, beyond elemental associations, honeybees are able to process configural associations. Bees were trained in a positive and anegative patterning discrimination problem. In the first problem, single odorants were nonreinforced whereas the compound was reinforced. In the second problem, single odorants were reinforced whereas the compound was nonreinforced. We studied whether bees can solve these problems and whether the ratio between the number of presentations of the reinforced stimuli and the number of presentations of the nonreinforced stimuli affects discrimination. Honeybees differentiated reinforced and nonreinforced stimuli in positive and negative patterning discriminations. They thus can process configural associations. The variation of the ratio of reinforced to nonreinforced stimuli modulated the amount of differentiation. The assignment of singular codes to complex odor blends could be implemented at the neural level: When bees are stimulated with odor mixtures, the activation patterns evoked at the primary olfactory neuropile, the antennal lobe, may be combinations of the single odorant responses that are not necessarily fully additive.

Figure 1

Conditioned proboscis extension response (% PER) across trials of a positive patterning discrimination. (a) Averaged % PER across all trials of A−, B−, and AB+ for Group PP1/1 (left), Group PP1/2 (middle), and Group PP1/5 (right). (b) Course of % PER to the nonreinforced elements (CSs−; filled circles) and to the reinforced compound (CS+; open circles). The upper panel shows responding for Group PP1/1, with a ratio of 1/1 between the number of presentations of the reinforced compound and the nonreinforced elements. Data were blocked to obtain six blocks of two CS− trials and six blocks of two CS+ trials. The middle panel shows responding for Group PP1/2 with a ratio of 1/2 of reinforced and nonreinforced trials. Data were blocked to obtain eight blocks of two CS− trials and eight blocks of one CS+ trial. The lower panel shows responding for Group PP1/5, with a ratio of 1/5 between the number of presentations of the reinforced compound and the nonreinforced elements. Data were blocked to obtain four blocks of five CS− trials and four blocks of one CS+ trial.

Figure 2

Conditioned proboscis extension response (% PER) across trials of a negative patterning discrimination. (a) Averaged % PER across all trials of A+, B+, and AB− for Group NP1/1 (left), Group NP1/2 (middle), and Group NP1/3 (right). (b) Course of % PER to the reinforced elements (CSs+; open circles) and to the nonreinforced compound (CS−; filled circles). The upper panel shows responding for Group NP1/1, with a ratio of 1/1 between the number of presentations of the reinforced elements and the nonreinforced compound. Data were blocked to obtain six blocks of two CS+ trials and six blocks of two CS− trials. The middle panel shows responding for Group NP1/2 with a ratio of 1/2 of reinforced and nonreinforced trials. Data were blocked to obtain four blocks of two CS+ trials and four blocks of four CS− trials. The lower panel shows responding for Group NP1/3 with a ratio of 1/3 of reinforced and nonreinforced trials. Data were blocked to obtain three blocks of two CS+ trials and three blocks of six CS− trials.