Towards plant-odor-related olfactory neuroethology in Drosophila

Abstract

Drosophila melanogaster is today one of the three foremost models in olfactory research, paralleled only by the mouse and the nematode. In the last years, immense progress has been achieved by combining neurogenetic tools with neurophysiology, anatomy, chemistry, and behavioral assays. One of the most important tasks for a fruit fly is to find a substrate for eating and laying eggs. To perform this task the fly is dependent on olfactory cues emitted by suitable substrates as e.g. decaying fruit. In addition, in this area, considerable progress has been made during the last years, and more and more natural and behaviorally active ligands have been identified. The future challenge is to tie the progress in different fields together to give us a better understanding of how a fly really behaves. Not in a test tube, but in nature. Here, we review our present state of knowledge regarding Drosophila plant-odor-related olfactory neuroethology to provide a basis for new progress.

Fig. 1

Scheme of odorant signal transduction. The insect odorant receptor complex is composed of an odorant-specific receptor protein OrX and the non-selective cation channel Or83 that conducts Na⁺, K⁺ and Ca²⁺. Odor-stimulation of OrX activates Or83 by an ionotropic and a metabotropic pathway. The direct activation of Or83b by OrX (red flash) leads to a fast and transient cation flow. The metabotropic pathway stimulates—via activation of G_s proteins by OrX—the adenylyl cyclase (AC) activity (violet flash) and thus the cAMP production. cAMP in turn activates Or83b (blue-green flash). The ionotropic pathway ensures a very rapid recognition of high odor concentrations while the metabotropic pathway allows highly sensitive odor detection

Fig. 2

Schematic of the Drosophila olfactory pathway. a Antennal olfactory sensory neurons (OSN, blue) converge in specific glomeruli of the antennal lobe. Some of them send an axonal branch through the antennal commissure to the other hemisphere. Local interneurons (LN, green) branch in all glomeruli and interconnect these with each other. Projections neurons (PN, red) collect the olfactory information within the antennal lobe and send their axons to higher processing centers as the calyx and the lateral protocerebrum. b Circuit diagram of the antennal lobe. The three principal populations of neurons and their synaptic connections within the glomeruli (gray circles) are represented. The diagram summarizes anatomical data from several insect species. Excitatory synapses are symbolised by triangles, inhibitory synapses by bars. In Drosophila, the existence of both inhibitory local interneurons (iLN) as well as excitatory local interneurons (eLN) has been shown

Fig. 3

Odors evoke specific patterns of glomerular activity in the Drosophila antennal lobe. The calcium-sensitive protein G-CaMP has been genetically expressed in either projection neurons (above) or sensory neurons (below). Calcium signals to two different odors have been superimposed onto the morphological image of the antennal lobe. Both odors lead to a specific, but different pattern of activated glomeruli. The activities are bilaterally symmetric between the left and the right antennal lobe. Comparison of the activity patterns between the sensory and the projection neurons to the same odor reveals similar but not identical responses

Fig. 4

Steck-Knaden assay. A 16 individually tracked flies are exposed to a clean-air flow. a–c A computer-controlled stimulus device generates odor stimuli, that meet the flies at a predictable time. When encountering an attractive odor, flies walk upwind. The tracking system calculates upwind speed before and after the stimulus reaches the fly. B Wind tunnel. d Flies show crosswind flights when exposed to clean-air flow. e When getting in contact with an odor plume, flies start upwind flights. A 3-D tracking system detects the time of plume contact and plume loss and calculates the flight’s directionality and upwind speed before and afterwards