Odor generalisation versus discrimination driven by a connectivity bias for different ethological groups of odors in the Drosophila Mushroom Body
1 Institute of Developmental Biology, RWTH Aachen University, Aachen, Germany
2 Neural Network Dynamics and Computation, Institute of Genetics, University of Bonn
The mushroom body (MB), the centre for olfactory associative learning in insect brain, performs pattern separation to discriminate between similar odors. We investigated mechanisms of odor discrimination in the Drosophila MB by combining connectome analysis, functional imaging, and network modelling. We found that the functional connections in MB deviates from the suggested optimum for odor discrimination and that different subtypes of MB neurons (MBNs) sample the olfactory space in distinctive ways. MBNs receive combinatorial input from various types of olfactory projection neurons (PNs). In the presence of inhibition, MBNs exhibit sparse population coding. The connection from PNs to MBNs determines the MBNs' pattern separation capabilities: it is theoretically optimal when MBNs receive random inputs from PNs. Contrary to the common assumption that MBN subtypes receive similar information about odors for various memory processes, our analysis of multiple connectomes revealed that α/β and α'/β' MBNs receive highly biased inputs from food-odor-responsive PNs, while γ MBNs receive slightly biased inputs from mating-odor-responsive PNs. By recording functional activity at MBNs’ soma, we showed that α/β and α'/β' MBNs form distinctly separated representations of food group odors and mating group odors. Additionally, within each odor group, odor representations are inherently clustered in the representational space of MBNs. By developing a MB network model that incorporates realistic PN-to-MBN-subtype connections, we showed that biased connection of α/β and α'/β' MBNs to food-odor-responsive PNs could increase their response overlap for food odors, when compared to random connections. Overall, these results suggest that the connections of α/β and α'/β' MBNs promote the generalisation of odors within the same ethological group such as feeding and mating, whereas γ MBNs, which do not show ethological groupings in their odor space, might enhance odor discrimination.