Olfactory Loss Enhances Visual Learning in Drosophila through Structural and Functional Reorganisation

Abstract

Loss of a sensory modality can enhance performance in the remaining senses. However, the circuit mechanisms by which such cross-modal compensation can improve cognitive functions, including learning, are unknown. Here, we show that compromising olfaction in both larval and adult Drosophila enhances visual associative learning. Using behavioural analysis, functional imaging, and comparative connectomics, we reveal the circuit mechanisms that underlie this improvement. Animals with improved learning ability have enhanced responses to visual stimuli in the higher-order learning circuit. The complementary circuit mechanisms that can enhance these responses are structural reweighting of inputs in the larva, resulting in an increased fraction of synaptic inputs from visual pathways onto neurons in the learning circuit, and a reduction in cross-modal inhibition in the adult. Together, these findings reveal synaptic and disinhibitory circuit mechanisms that enhance learning in higher-order associative networks following sensory loss.