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Context generalization in Drosophila visual learning requires the mushroom bodies

Abstract

The world is permanently changing. Laboratory experiments on learning and memory normally minimize this feature of reality, keeping all conditions except the conditioned and unconditioned stimuli as constant as possible1. In the real world, however, animals need to extract from the universe of sensory signals the actual predictors of salient events by separating them from non-predictive stimuli (context2). In principle, this can be achieved ifonly those sensory inputs that resemble the reinforcer in theirtemporal structure are taken as predictors. Here we study visual learning in the fly Drosophila melanogaster, using a flight simulator3,4, and show that memory retrieval is, indeed, partially context-independent. Moreover, we show that the mushroom bodies, which are required for olfactory5,6,7 but not visual or tactile learning8, effectively support context generalization. In visual learning in Drosophila, it appears that a facilitating effect of context cues for memory retrieval is the default state, whereas making recall context-independent requires additional processing.

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Figure 1: Experimental set-up and procedure.
Figure 2: Influence of colour changes on memory retrieval.
Figure 3: Context changes between dark flash (DF) condition and no dark flashes.
Figure 4: Stimulus generalization occurs in flies without mushroom bodies.

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Acknowledgements

We thank S. Kramer for critically reading the manuscript; S. Clemens-Richter for technical help; T. Raabe for the enhancer-trap line P[Gal4]17D; S. T. Sweeney and C. J. O'Kane for the UASGal4–CntE stock; and J. Thierer and H. Niemann for tetanus toxin antibody. The work has been supported by Deutsche Forschungsgemeinschaft, Fond der Chemischen Industrie (M.H.) and Alexander von Humboldt-Foundation (L.L.).

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Correspondence to Martin Heisenberg.

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Liu, L., Wolf, R., Ernst, R. et al. Context generalization in Drosophila visual learning requires the mushroom bodies. Nature 400, 753–756 (1999). https://doi.org/10.1038/23456

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