Non-synaptic interactions between olfactory receptor neurons, a possible key feature of odor processing in flies

When flies explore their environment, they encounter odors in complex, highly intermittent plumes. To navigate a plume and, for example, find food, they must solve several challenges, including reliably identifying mixtures of odorants and their intensities, and discriminating odorant mixtures emanating from a single source from odorants emitted from separate sources and just mixing in the air. Lateral inhibition in the antennal lobe is commonly understood to help solving these challenges. With a computational model of the Drosophila olfactory system, we analyze the utility of an alternative mechanism for solving them: Non-synaptic (“ephaptic”) interactions (NSIs) between olfactory receptor neurons that are stereotypically co-housed in the same sensilla. We find that NSIs improve mixture ratio detection and plume structure sensing and do so more efficiently than the traditionally considered mechanism of lateral inhibition in the antennal lobe. The best performance is achieved when both mechanisms work in synergy. However, we also found that NSIs decrease the dynamic range of co-housed ORNs, especially when they have similar sensitivity to an odorant. These results shed light, from a functional perspective, on the role of NSIs, which are normally avoided between neurons, for instance by myelination.

Predictive Coding, Variational Autoencoders, and Biological Connections

We present a review of predictive coding, from theoretical neuroscience, and variational autoencoders, from machine learning, identifying the common origin and mathematical framework underlying both areas. As each area is prominent within its respective field, more firmly connecting these areas could prove useful in the dialogue between neuroscience and machine learning. After reviewing each area, we discuss two possible correspondences implied by this perspective: cortical pyramidal dendrites as analogous to (nonlinear) deep networks and lateral inhibition as analogous to normalizing flows. These connections may provide new directions for further investigations in each field.

Role of Lateral Inhibition on Visual Number Sense

Lateral inhibition is a basic principle of information processing and widely exists in the human and animal nervous systems. Lateral inhibition is also involved in processing visual information because it travels through the retina, primary visual cortex, and visual nervous system. This finding suggests that lateral inhibition is associated with visual number sense in humans and animals. Here, we show a number-sensing neural network model based on lateral inhibition. The model can reproduce the size and distance effects of the output response of human and animal number-sensing neurons when the network connection weights are set randomly without adjustment. The number sense of the model disappears when lateral inhibition is removed. Our study shows that the first effect of lateral inhibition is to strengthen the linear correlation between the total response intensity of the input layer and the number of objects. The second one is to allow the output cells to prefer different numbers. Results indicate that lateral inhibition plays an indispensable role in untrained spontaneous number sense.

Connectivity and dynamics in the olfactory bulb

Dendrodendritic interactions between excitatory mitral cells and inhibitory granule cells in the olfactory bulb create a dense interaction network, reorganizing sensory representations of odors and, consequently, perception. Large-scale computational models are needed for revealing how the collective behavior of this network emerges from its global architecture. We propose an approach where we summarize anatomical information through dendritic geometry and density distributions which we use to calculate the probability of synapse between mitral and granule cells, while capturing activity patterns of each cell type in the neural dynamical systems theory of Izhikevich. In this way, we generate an efficient, anatomically and physiologically realistic large-scale model of the olfactory bulb network. Our model reproduces known connectivity between sister vs. non-sister mitral cells; measured patterns of lateral inhibition; and theta, beta, and gamma oscillations. It in turn predicts testable relations between network structure, lateral inhibition, and odor pattern decorrelation; between the density of granule cell activity and LFP oscillation frequency; how cortical feedback to granule cells affects mitral cell activity; and how cortical feedback to mitral cells is modulated by the network embedding. Additionally, the methodology we describe here provides a tractable tool for other researchers.