Subjective rather than absolute reward value determines long-term memory formation in honey bees

Abstract

How animals evaluate reward quality is a fundamental question in neuroscience and behavioral biology. Here we show that in honey bees (Apis mellifera), the value of a sucrose reward is not processed in absolute terms but relative to prior experience, and that this subjective evaluation strongly influences long-term memory formation. Using appetitive olfactory conditioning of the proboscis extension reflex (PER), we demonstrate that memory performance is determined by the contrast between a previously experienced reward and the reward used during training, rather than by the absolute concentration of sucrose received. This effect operates across multiple timescales, from contrasts between successive trials within a single session to differences between rewards experienced 24 hours apart. We further show that prior exposure to sucrose solutions of different concentrations modulates gustatory responsiveness and alters the sensitivity of antennal gustatory receptor neurons, suggesting that peripheral sensory plasticity contributes to experience-dependent changes in reward evaluation. Dissociating pre- and post-ingestive reward components revealed that the contrast between the sucrose concentration sensed by the antennae and the concentration ingested is sufficient to modulate memory formation. Together, our results indicate that bees form an internal expectation of reward quality based on experience, and that this expectation rescales the perceived value of subsequent rewards, thereby shaping associative memory strength. These findings provide a mechanistic framework for understanding how invertebrates perform relative reward comparisons across multiple temporal scales, with implications for flexible foraging strategies in dynamic environments.