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Analysis of a spatial orientation memory in Drosophila

Abstract

Flexible goal-driven orientation requires that the position of a target be stored, especially in case the target moves out of sight. The capability to retain, recall and integrate such positional information into guiding behaviour has been summarized under the term spatial working memory1. This kind of memory contains specific details of the presence that are not necessarily part of a long-term memory. Neurophysiological studies in primates2 indicate that sustained activity of neurons encodes the sensory information even though the object is no longer present. Furthermore they suggest that dopamine transmits the respective input to the prefrontal cortex, and simultaneous suppression by GABA spatially restricts this neuronal activity3. Here we show that Drosophila melanogaster possesses a similar spatial memory during locomotion. Using a new detour setup, we show that flies can remember the position of an object for several seconds after it has been removed from their environment. In this setup, flies are temporarily lured away from the direction towards their hidden target, yet they are thereafter able to aim for their former target. Furthermore, we find that the GABAergic (stainable with antibodies against GABA) ring neurons4 of the ellipsoid body in the central brain are necessary and their plasticity is sufficient for a functional spatial orientation memory in flies. We also find that the protein kinase S6KII (ignorant)5 is required in a distinct subset of ring neurons to display this memory. Conditional expression of S6KII in these neurons only in adults can restore the loss of the orientation memory of the ignorant mutant. The S6KII signalling pathway therefore seems to be acutely required in the ring neurons for spatial orientation memory in flies.

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Figure 1: Orientation memory in the detour paradigm.
Figure 2: The ellipsoid-body ring neurons are necessary for orientation memory.
Figure 3: S6KII activity is necessary for orientation memory.
Figure 4: S6KII activity in the ring neurons is sufficient to restore orientation memory.

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Acknowledgements

We thank M. Heisenberg for discussions and continuous support, D. Kretzschmar for reading the manuscript, and E. Stepien-Bötsch for experimental contributions. This work was supported by the Deutsche Forschungsgemeinschaft (SFB 554-B7, GRK 1156).

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Correspondence to Roland Strauss.

Supplementary information

The file contains Supplementary Figures S1-S3 and Legends and Supplementary Table S1 on Statistics

The file shows additional data on the persistence of orientation in mutant lines with structural central complex defects (Figure S1), immunohistological preparations showing no thoracic expression of GAL4-lines c232, c481 and c105 (Figure S2), the locomotor and orientation behaviour of wild-type Canton-S and ign58/1 mutant flies in Buridan`s paradigm (Figure S3), and Supplementary Table S1 on statistics. (PDF 231 kb)

The file contains Supplementary Movie 1 which shows wild-type Canton-S male performing the detour paradigm in real-time

The fly (arrow) approaches the left stripe. The initial target automatically disappears, while laterally to the fly (in the upper half of the screen) another vertical stripe appears as distracter. As soon as the fly has turned toward this distracter with less than 15° deviation, the distracter will disappear as well within 1s. The fly reorients towards the position of its former target and eventually shows random search behaviour. (MOV 15310 kb)

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Neuser, K., Triphan, T., Mronz, M. et al. Analysis of a spatial orientation memory in Drosophila. Nature 453, 1244–1247 (2008). https://doi.org/10.1038/nature07003

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