Distinct signaling of Drosophila chemoreceptors in olfactory sensory neurons

Significance Drosophila is a popular model system for the study of olfaction. However, the physiological properties of its olfactory sensory neurons, both intrinsic and responsive, remain unclear. We have succeeded, for the first time, in patch-clamp recording from targeted Drosophila OSNs, revealing the distinct signaling of odorant receptors (Ors) and ionotropic receptors (Irs). We found that Ir-driven receptor currents did not adapt, whereas Or responses strongly adapted. Surprisingly, although Or adaptation increased odor sensitivity at high odor backgrounds, it reduced odor sensitivity at low backgrounds. Adaptation permeates all senses, and the finding of dynamic gain control by adaptation in Drosophila Or-expressing OSNs sheds light on the understanding of adaptation in other sensory systems. In Drosophila, olfactory sensory neurons (OSNs) rely primarily on two types of chemoreceptors, odorant receptors (Ors) and ionotropic receptors (Irs), to convert odor stimuli into neural activity. The cellular signaling of these receptors in their native OSNs remains unclear because of the difficulty of obtaining intracellular recordings from Drosophila OSNs. Here, we developed an antennal preparation that enabled the first recordings (to our knowledge) from targeted Drosophila OSNs through a patch-clamp technique. We found that brief odor pulses triggered graded inward receptor currents with distinct response kinetics and current–voltage relationships between Or- and Ir-driven responses. When stimulated with long-step odors, the receptor current of Ir-expressing OSNs did not adapt. In contrast, Or-expressing OSNs showed a strong Ca2+-dependent adaptation. The adaptation-induced changes in odor sensitivity obeyed the Weber–Fechner relation; however, surprisingly, the incremental sensitivity was reduced at low odor backgrounds but increased at high odor backgrounds. Our model for odor adaptation revealed two opposing effects of adaptation, desensitization and prevention of saturation, in dynamically adjusting odor sensitivity and extending the sensory operating range.