Octopamine improves learning in newly emerged bees but not in old foragers

Abstract

SUMMARYHoney bees (Apis mellifera) are well known for their excellent learning abilities. Although most age groups learn quickly to associate an odor with a sucrose reward, newly emerged bees and old foragers often perform poorly. For a long time, the reason for the poor learning performance of these age groups was unclear. We show that reduced sensitivity for sucrose is the cause for poor associative learning in newly emerged bees but not in old foragers. By increasing the sensitivity for sucrose through octopamine, we selectively improved the learning performance of insensitive newly emerged bees. Interestingly, the learning performance of foragers experiencing the same treatment remained low, despite the observed increase in sensitivity for the reward. We thus demonstrate that increasing sensitivity for the reward can improve the associative learning performance of bees when they are young but not when they had foraged for a long time. Importantly, octopamine can have very different effects on bees, depending on their initial sensory sensitivity. These differential effects of octopamine have important consequences for interpreting the action of biogenic amines on insect behavior.

Learning, gustatory responsiveness and tyramine differences across nurse and forager honeybees

“…perception of the sucrose reward in a water solution. Indeed, we could demonstrate that increasing gustatory responsiveness through pharmacological activation of octopamine receptors suffices to improve appetitive learning performance in young bees (Behrends and Scheiner, 2012). Our current results provide further support for the hypothesis that there is a causal relationship between gustatory responsiveness and appetitive PER learning in honeybees by ) into the hemolymph (tyramine titer: n control =9, n tyramine =7, octopamine titer: n control =10, n tyramine =7).…”

“…The behavioral changes of tyramine that are similar to those of octopamine might be achieved through the second honeybee tyramine receptor, AmTYR2, which acts similarly to the octopamine receptors AmOCTβR1 to AMOCTβR4 (Balfanz et al, 2014;Reim et al, 2017) by upregulating cAMP. Octopamine similarly improves appetitive learning performance in honeybees, as does tyramine (Behrends and Scheiner, 2012). However, these are pure speculations.…”

“…As tyramine is the metabolic precursor of octopamine, the higher tyramine titer might not directly cause behavioral changes, but additional tyramine may be converted into octopamine. Similar to tyramine, octopamine was shown to increase gustatory responsiveness in honeybees (Scheiner et al, 2002;Behrends and Scheiner, 2012). Ultimately, experiments manipulating the expression of specific tyramine and octopamine receptors (Farooqui et al, 2003) will help to separate the role of octopamine and tyramine and to attribute behavioral changes during the nurse-forager transition to specific receptor types.…”

“…Tyramine might further have independent effects on gustatory responsiveness and learning performance, which only become apparent in foragers. Interestingly, octopamine can improve the learning performance of young bees but not of old foragers, very similar to tyramine and even though octopamine increases gustatory responsiveness in old foragers (Behrends and Scheiner, 2012). It is therefore conceivable that after a certain time window in adult development, tyramine and octopamine may not be able to affect cognitive-like functions any longer, even though they can modulate gustatory responsiveness.…”

Rapid learning dynamics in individual honeybees during classical conditioning

“…For the honeybee, several studies showed that factors such as satiation level, behavioral role or age have an effect on individual responsiveness for sucrose, which in turn affects learning performance (Scheiner et al, 1999; Friedrich et al, 2004; Behrends and Scheiner, 2012). Re-analyzing data in which the responsiveness to sucrose was estimated prior to conditioning we studied the correlation between this experimental measure and the individual learning dynamics.…”