Plasticity in inhibitory networks improves pattern separation in early olfactory processing

Distinguishing between nectar and non-nectar odors is challenging for animals due to shared compounds and varying ratios in complex mixtures. Changes in nectar production throughout the day - and potentially many times within a forager’s lifetime - add to the complexity. The honeybee olfactory system, containing fewer than 1,000 principal neurons in the early olfactory relay, the antennal lobe (AL), must learn to associate diverse volatile blends with rewards. Previous studies identified plasticity in the AL circuits, but its role in odor learning remains poorly understood. Using a biophysical computational network model, tuned by in vivo electrophysiological data, and live imaging of the honeybee’s AL, we explored the neural mechanisms and functions of plasticity in the early olfactory system. Our findings revealed that when trained with a set of rewarded and unrewarded odors, the AL inhibitory network suppresses shared chemical compounds while enhancing responses to distinct compounds. This results in improved pattern separation and a more concise neural code. Our calcium imaging data support these predictions. Analysis of a graph convolutional neural network performing an odor categorization task revealed a similar mechanism for contrast enhancement. Our study provides insights into how inhibitory plasticity in the early olfactory network reshapes the coding for efficient learning of complex odors. Significance Statement By combining biophysical modeling, machine learning, electrophysiology and analysis of calcium imaging data, we demonstrate that associative and nonassociative plasticity in the honeybee antennal lobe (AL) the first relay of the insect olfactory system - work together to enhance the contrast between rewarded and unrewarded odors. Training the AL’s inhibitory network within specific odor environments enables the suppression of neural responses to common odor components while amplifying responses to distinctive ones. This study sheds light on the olfactory system’s ability to adapt and efficiently learn new odor-reward associations across varying environments, and it proposes innovative, energy-efficient principles applicable to artificial intelligence.