Response competition associated with right–left antennal asymmetries of new and old olfactory memory traces in honeybees

Abstract

Lateralized recall of olfactory memory in honeybees was tested, following conditioning of the proboscis extension reflex (PER), at 1 or 6 h after training. After training with lemon (+)/vanilla (−) or cineol (+)/eugenol (−) recall at 1 h was better when the odour was presented to the right side of the bee than when it was presented to the left side. In contrast, recall at 6 h was better when the odour was presented to the left than to the right side. This confirmed previous evidence of shorter-term recall via the right antenna and long-term memory recall via the left antenna. However, when trained with either a familiar appetitive odour (rose) as a negative stimulus, or with a naturally aversive odour (isoamyl acetate, IAA) as a positive stimulus, bees showed suppression of the response from both the right and the left side at 1 h after training (likely due to retroactive inhibition) and at 6 h responded to both odours on both sides. We argued that at 6 h, when access to memory has completed the shift from the right to the left side, memory of these familiar odours in the left side of the brain would be present as both positive (rose)/negative (IAA) (as a result of long-term memory either biologically encoded or acquired well before testing) and negative (rose)/positive (IAA) (as a result of the long-term memory of training) stimuli, thus producing response competition. As a direct test of this hypothesis, bees were first trained with unfamiliar lemon (+)/vanilla (−) and then (16 h later) re-trained with vanilla (+)/lemon (−); as predicted, 6 h after re-training bees responded to both odours on both the left and right side.