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Associative learning plays a fundamental role in the life of honey bees, especially in the context of foraging for food sources. This learning capacity can be investigated through controlled experiments conducted under laboratory, semi-natural, and near-natural conditions, to understand the general principles of learning and motivation. Honey bees can be trained to solve different elemental and non-elemental learning tasks by pairing a conditioned stimulus such as an odor with sucrose as an unconditioned stimulus and reward. Laboratory studies with restrained bees demonstrated that sucrose responsiveness is positively correlated with both elemental olfactory learning performance and responsiveness to stimuli of different sensory modalities, such as odors and visual stimuli. Here, we tested for the first time how responsiveness to sucrose and light is related to performance in elemental and non-elemental visual learning under free-flying conditions. Sensory responsiveness and learning proficiency did not correlate, nor did sucrose responsiveness correlate with responsiveness to light. These results indicate that relationships among responsiveness to sucrose and light and learning proficiency, as established under restrained laboratory conditions, may not translate to the natural behavior of bees in the field. This finding points toward the context-dependent importance of responsiveness to light and sucrose during associative learning under restrained or free-flying conditions.

The pathways for olfactory learning in the fruitfly Drosophila have been extensively investigated, with mounting evidence that that the mushroom body is the site of the olfactory associative memory trace (Heisenberg, Nature 4:266–275, 2003 ; Gerber et al., Curr Opin Neurobiol 14:737–744, 2004 ). Heisenberg’s description of the mushroom body as an associative learning device is a testable hypothesis that relates the mushroom body’s function to its neural structure and input and output pathways. Here, we formalise a relatively complete computational model of the network interactions in the neural circuitry of the insect antennal lobe and mushroom body, to investigate their role in olfactory learning, and specifically, how this might support learning of complex (non-elemental; Giurfa, Curr Opin Neuroethol 13:726–735, 2003 ) discriminations involving compound stimuli. We find that the circuit is able to learn all tested non-elemental paradigms. This does not crucially depend on the number of Kenyon cells but rather on the connection strength of projection neurons to Kenyon cells, such that the Kenyon cells require a certain number of coincident inputs to fire. As a consequence, the encoding in the mushroom body resembles a unique cue or configural representation of compound stimuli (Pearce, Psychol Rev 101:587–607, 1994 ). Learning of some conditions, particularly negative patterning, is strongly affected by the assumption of normalisation effects occurring at the level of the antennal lobe. Surprisingly, the learning capacity of this circuit, which is a simplification of the actual circuitry in the fly, seems to be greater than the capacity expressed by the fly in shock-odour association experiments (Young et al. 2010 ).