Distinct signaling of Drosophila chemoreceptors in olfactory sensory neurons

Abstract

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 Ca 2+ -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.Drosophila | olfaction | chemoreceptor | sensory adaptation | OSN

Olfactory receptor neurons use gain control and complementary kinetics to encode intermittent odorant stimuli

“…In ORNs, transduction currents elicited by odorant pulses are reduced by preceding pulses (Nagel and Wilson, 2011) and scale inversely with background intensity, consistent with the Weber-Fechner law (Cafaro, 2016; Cao et al, 2016). It remains unclear whether the ORNs’ ultimate output — the firing rate — follows the same Weber-Fechner scaling (Cafaro, 2016; Martelli et al, 2013).…”

“…To quantify these differences, we defined the gain of the neuron to be the change in the response for a unit change in the stimulus ($true0gain:=\mathrm{\Delta }R/\mathrm{\Delta }S$). Since ORNs do not respond instantaneously to odorant stimuli (Cao et al, 2016; de Bruyne et al, 2001; Martelli et al, 2013; Nagel and Wilson, 2011) we fit linear filters to best predict the LFP and firing rate from the stimulus. We used these filters to make linear predictions of the responses from the stimuli (Figure 1—figure supplement 4).…”

“…In olfaction, the Weber-Fechner Law was demonstrated at the LFP level (Cafaro, 2016; Cao et al, 2016). Here we directly measured ORN firing rate and stimulus intensity and found that the ORN firing rate exhibited Weber-Fechner gain scaling relative to the mean stimulus intensity for five different odor-receptor combinations (Figure 3, Figure 3—figure supplement 1).…”

Goggatomy: a Method for Opening Small Cuticular Compartments in Arthropods for Physiological Experiments

“…It might be possible to make intracellular recording from the component cells of scolopidia with an appropriate sharp electrode, perhaps quartz or by digesting the extracellular matrix with proteases. Our confidence that intracellular recordings can be made from Drosophila JO is bolstered by reports of whole-cell and perforated patch recordings from ORNs in A3s that have been cut open (Dubin and Harris, 1997;Cao et al, 2016).…”

Adaptation in Living Systems

“…Once R is determined, then all responses of the adaptive wild-type (WT) cells in any given backgrounds can be determined by just two parameters K 0 and λ . This approach has been used successfully to explain response sensitivities in both the rhodopsine and the olfactory neurons (87). …”