Elements of Olfactory Intelligence in Drosophila

The ability to make the world of odorants intelligible is a key capability of the Drosophila olfactory system that we shall call olfactory intelligence. We argue that olfactory intelligence does not only arise in the form of associative learning in the Mushroom Body, but can be seen throughout the first three stages of the early olfactory system: the Antenna, the Antennal Lobe and the Mushroom Body Calyx, where encoding and processing of odorants take places. Characterizing the structure and logic of the code underlying the spike trains accessing the memory in the Mushroom Body is a major challenge in neuroscience. To address this challenge and unveil the key elements of olfactory intelligence, we extensively model the function of the Drosophila early olfactory system from its intriguing connectome. We start by modeling the space of odorants using constructs of both semantic and syntactic information. Odorant semantics concerns the identity of odorants while odorant syntax pertains to their concentration amplitude. These odorant attributes are multiplicatively coupled in the process of olfactory transduction. To make the world of odorants intelligible, we establish that the Drosophila Antennal Lobe and Calyx largely reduce the concentration dependency of the odorant information from the confounding representation of the Antenna, and thereby disentangle the odorant semantic information from the odorant syntactic information. We also introduce a novel time and rank-based representation of Kenyon Cell (KC) outputs, called the marked first spike sequence code. We compare the cumulative inter-spike interval statistics of odorant semantics and introduce a novel distance measure for the accurate classification of odorant semantics. Computationally, these elements of olfactory intelligence are realized by a class of differential divisive normalization processors (DNPs) modeling the feedback circuits in the Antennal Lobe facilitated by Local Neurons and in the Calyx by the Anterior Paired Lateral (APL) neuron. The marked first spike sequence code at the output of the DNP circuit of the Calyx provides a novel representation of the odorant semantics. The code reflects the amplitude ranking that drives the KCs in the time domain. Strikingly, the APL feedback not only removes the con-centration dependency of the KC outputs, but also increases the ranking distance between the marked first spike sequence codes representing different odorant identities. Thus, the rank-based representation supports accurate classification of odorant semantics.