Abstract
Insects detect volatile chemicals using antennae, which house a vast variety of olfactory sensory neurons (OSNs) that innervate hair-like structures called sensilla where odor detection takes place. In addition to OSNs, the antenna also hosts various support cell types. These include the triad of trichogen, tormogen, and thecogen support cells that lie adjacent to their respective OSNs. The arrangement of OSN supporting cells occurs stereotypically for all sensilla and is widely conserved in evolution. While insect chemosensory neurons have received considerable attention, little is known about the functional significance of the cells that support them. For instance, it remains unknown whether support cells play an active role in odor detection, or only passively contribute to homeostasis, e.g., by maintaining sensillum lymph composition. To investigate the functional interaction between OSNs and support cells, we used optical and electrophysiological approaches in Drosophila. First, we characterized the distribution of various supporting cells using genetic markers. By means of an ex vivo antennal preparation and genetically-encoded Ca2+ and K+ indicators, we then studied the activation of these auxiliary cells during odor presentation in adult flies. We observed acute responses and distinct differences in Ca2+ and K+ fluxes between support cell types. Finally, we observed alterations in OSN responses upon thecogen cell ablation in mature adults. Upon inducible ablation of thecogen cells, we notice a gain in mechanical responsiveness to mechanical stimulations during single-sensillum recording, but a lack of change to the neuronal resting activity. Taken together, these results demonstrate that support cells play a more active and responsive role during odor processing than previously thought. Our observations thus reveal that support cells functionally interact with OSNs and may be important for the extraordinary ability of insect olfactory systems to dynamically and sensitively discriminate between odors in the turbulent sensory landscape of insect flight.
Highlights
Olfaction is an ancient and critical sensory modality for all animals
We found no mechanoreceptor potential A (nompA) exclusively at the base of the sensillum (Supplementary Figure 1A), suggesting that nompA does not interact at the odor-receptor interface but rather acts as an extracellular scaffold or matrix component likely holding olfactory sensory neurons (OSNs) dendrites in place
We asked whether the marker would occur in ab3 sensilla, in different morphological types of sensilla, as well as whether they would occur in Orco-negative sensory neurons expressing ionotropic receptor (IR), such as those found in coeloconic sensilla of the sacculus
Summary
Sensitivity to volatile chemicals underpins a great variety of essential behaviors for survival and reproduction such as foraging for food, avoidance of biotic and abiotic hazards, sexual mating, reception of inter- and intraspecific semiochemicals (Vosshall, 2000), and is both ubiquitous and principal sense for metazoan life (Ache and Young, 2005). Though the astounding variety of smelling organs may seem diverse, the general features of olfactory systems are conserved and share several invariable features which allow for specific and sensitive sampling of broad ranges of odors (Eisthen, 1997; Krieger and Breer, 1999; Ache and Young, 2005; Eisthen and Polese, 2007; Ng et al, 2020). With respect to the cellular repertoire, olfactory organs are always composed of odorant receptor-equipped sensory neurons innervating an epithelium, and a lesser-explored set of auxiliary cells that co-arise in development, which remain closely apposed to their corresponding neurons, and are thought to play roles in maintaining and potentiating the ability of neurons to perform their sensory function (Schmidt and Benton, 2020)
Sign-in/Register to view highlights & summary Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
