In a permanently changing environment, it is by no means an easy task to distinguish potentially important events from negligible ones. Yet, to survive, every animal has to continuously face that challenge. How does the brain accomplish this feat? Building on previous work in Drosophila melanogaster visual learning, we have developed an experimental methodology in which combinations of visual stimuli (colors and patterns) can be arranged such that the same stimuli can either be directly predictive, indirectly predictive, or nonpredictive of punishment. Varying this relationship, we found that wild-type flies can establish different memory templates for the same contextual color cues. The colors can either leave no trace in the pattern memory template, leading to context-independent pattern memory (context generalization), or be learned as a higher-order cue indicating the nature of the pattern-heat contingency leading to context-dependent memory (occasion setting) or serve as a conditioned stimulus predicting the punishment directly (simple conditioning). In transgenic flies with compromised mushroom-body function, the sensitivity to these subtle variations is altered. Our methodology constitutes a new concept for designing learning experiments. Our findings suggest that the insect mushroom bodies stabilize visual memories against context changes and are not required for cognition-like higher-order learning.
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