The functional logic of odor information processing in the Drosophila antennal lobe

Author SummaryA major challenge in the study of the Drosophila early olfactory sensory system is to determine how an odorant object (the smell of a rose) is reliably identified in the face of fluctuations of the concentration amplitude of the molecules within the odorant plume. More fundamentally, the question arises how semantic information, often associated with subjective perception, can be characterized. To address this challenge, we leveraged the unique combinatorial odorant code of Drosophila and presented a formal treatment of the identity of an odorant object as its semantic information (or semantics for short). Grounded in the physiology of the fly brain, we identified the functional roles played by Local Neurons in the fruit fly Antennal Lobe in the recovery of the semantics and the onset/offset timing information (or semantic timing). Our model of the Antennal Lobe circuit is built with a highly versatile canonical model of neural computation-the differential Divisive Normalization Processor. Recent advances in molecular transduction of odorants in the Olfactory Sensory Neurons (OSNs) of the Drosophila Antenna have shown that the odorant object identity is multiplicatively coupled with the odorant concentration waveform. The resulting combinatorial neural code is a confounding representation of odorant semantic information (identity) and syntactic information (concentration). To distill the functional logic of odor information processing in the Antennal Lobe (AL) a number of challenges need to be addressed including 1) how is the odorant semantic information decoupled from the syntactic information at the level of the AL, 2) how are these two information streams processed by the diverse AL Local Neurons (LNs) and 3) what is the end-to-end functional logic of the AL?By analyzing single-channel physiology recordings at the output of the AL, we found that the Projection Neuron responses can be decomposed into a concentration-invariant component, and two transient components boosting the positive/negative concentration contrast that indicate onset/offset timing information of the odorant object. We hypothesized that the concentration-invariant component, in the multi-channel context, is the recovered odorant identity vector presented between onset/offset timing events.We developed a model of LN pathways in the Antennal Lobe termed the differential Divisive Normalization Processors (DNPs), which robustly extract the semantics (the identity of the odorant object) and the ON/OFF semantic timing events indicating the presence/absence of an odorant object. For real-time processing with spiking PN models, we showed that the phase-space of the biological spike generator of the PN offers an intuit perspective for the representation of recovered odorant semantics and examined the dynamics induced by the odorant semantic timing events. Finally, we provided theoretical and computational evidence for the functional logic of the AL as a robust ON-OFF odorant object identity recovery processor across odorant identities, concentration amplitudes and waveform profiles.