A Molecular Odorant Transduction Model and the Complexity of Combinatorial Encoding in the Drosophila Antenna

Abstract

In the past two decades, substantial amount of work characterized the odorant receptors, neuroanatomy and odorant response properties of the early olfactory system of Drosophila melanogaster. Yet many odorant receptors remain only partly characterized, the odorant transduction process and the axon hillock spiking mechanism have yet to be fully determined.The essential functionality of olfactory sensory neurons (OSNs) is to jointly encode both odorant identity and odorant concentration. We model identity and concentration by an odorant-receptor binding rate tensor modulated by the odorant concentration profile and an odorant-receptor dissociation rate tensor, and quantitatively describe the ligand binding/dissociation process.To validate our modeling approach, we first propose an algorithm for estimating the affinity and the dissociation rate of an odorant-receptor pair. We then apply the algorithm to estimate the affinity and dissociation rate for (acetone, Or59b) using two different datasets of electrophysiology recordings. Second, we evaluate the temporal response of the Or59b OSN model to acetone with a multitude of stimuli, including step, ramp and parabolic odorant waveforms. We further interrogate the model with staircase and noisy waveforms.. CC-BY-NC-ND 4.0 International license peer-reviewed) is the author/funder. It is made available under aThe copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/237669 doi: bioRxiv preprint first posted online Dec. 21, 2017; 2 Lastly, we evaluate the affinity and the dissociation rate for different odorantreceptor pairs including (methyl butyrate, Or59b) and (butyraldehyde, Or7a).We demonstrate how to evaluate the odorant transduction process and biological spike generator cascade underlying the fruit fly OSN model at the circuit level of the antennae and maxillary palps under two scenarios. First, we empirically estimate the odorant-receptor affinity of the active receptor model in response to constant concentration odorants using the spike count records in the DoOR database. Second, we evaluate and graphically visualize the temporal response of the antennae and maxillary palps using a staircase odorant concentration waveform. Finally, we describe how to construct, execute and explore various instantiations of the antennae and maxillary palps as a parallel information preprocessor in the open-source Fruit Fly Brain Observatory platform.