Attention, Awareness, and Cognitive Flexibility in an Insect: Divergent Effects of Distraction on Delay and Trace Reversal Learning in Honey Bees

The question of whether awareness is required for trace conditioning, but not for delay conditioning, has recently been explored in the honey bee, a species renowned for its cognitive abilities. In this insect, distractors impaired trace but not delay absolute olfactory conditioning, suggesting that honey bees, like humans, rely on awareness of the CS-US contingency during trace learning. Here, we extend this approach to reversal learning, which requires abandoning previously learned associations and acquiring new ones. Bees mastered olfactory reversal learning under both delay and trace protocols. However, introducing a visual distractor during the reversal phase impaired performance in distinct ways. Delay-conditioned bees increased responsiveness, adopting a generalized response profile (A⁺B⁺), whereas trace-conditioned bees decreased responsiveness, adopting a non-responsive profile (A⁻B⁻). To our knowledge, this is the first study in any animal species to investigate reversal learning under a trace-conditioning regime, and the first to assess distractor effects in such a demanding paradigm. The contrasting outcomes indicate that the distractor disrupted attentional reallocation in both protocols, but additionally interfered with contingency awareness required in trace learning. These findings provide unprecedented evidence that honey bees engage awareness-like processes during trace reversal learning, highlighting intricate attentional and temporal processing in an insect.