Odor Coding in the Drosophila Antenna

Abstract

Odor coding in the Drosophila antenna is examined by a functional analysis of individual olfactory receptor neurons (ORNs) in vivo. Sixteen distinct classes of ORNs, each with a unique response spectrum to a panel of 47 diverse odors, are identified by extracellular recordings. ORNs exhibit multiple modes of response dynamics: an individual neuron can show either excitatory or inhibitory responses, and can exhibit different modes of termination kinetics, when stimulated with different odors. The 16 ORN classes are combined in stereotyped configurations within seven functional types of basiconic sensilla. One sensillum type contains four ORNs and the others contain two neurons, combined according to a strict pairing rule. We provide a functional map of ORNs, showing that each ORN class is restricted to a particular spatial domain on the antennal surface.

Dynamic Characterization ofDrosophilaAntennal Olfactory Neurons Indicates Multiple Opponent Signaling Pathways in Odor Discrimination

“…Both inhibitory and excitatory responses have been reported in insect primary olfactory neurons (de Bruyne et al, 2001;Shields and Hildebrand, 2001;Hallem et al, 2004;Tichy et al, 2005;Yao et al, 2005) and their odorant receptors . The frequency response approach allowed us to detect simultaneous excitation and inhibition in multiple neurons within a sensillum during the same stimulation by fluctuating concentrations of odorants.…”

“…Odor selectivities of individual sensory neurons are controlled, in part, by odorant receptor molecules in their distal dendrites (Couto et al, 2005;Hiroi et al, 2008). Significant attention has been focused on basiconic sensilla in the medial proximal region of the third segment (de Bruyne et al, 2001;Stensmyr et al, 2003;Hallem et al, 2004) because their sensitivity to fruit odors implies important behavioral roles and a window into central processing mechanisms.…”

“…Sensory neurons of basiconic sensilla generate background action-potential firing without olfactory stimulation (de Bruyne et al, 2001), allowing inhibitory reduction of firing in addition to the excitatory increase in firing that has been widely used to identify odorant specificity. Inhibitory responses in insect olfaction include cockroach antennal sensilla responding with opposite polarity to lemon oil (Tichy et al, 2005), Manduca sexta olfactory sensilla giving inhibitory responses to a range of odorants (Shields and Hildebrand, 2001), Drosophila basiconic and coeloconic sensilla inhibited by some food odorants and terpenes (de Bruyne et al, 2001;Yao et al, 2005), and Drosophila trichoid sensilla inhibited by fruit odorants (Hallem et al, 2004).…”

“…Inhibitory responses in insect olfaction include cockroach antennal sensilla responding with opposite polarity to lemon oil (Tichy et al, 2005), Manduca sexta olfactory sensilla giving inhibitory responses to a range of odorants (Shields and Hildebrand, 2001), Drosophila basiconic and coeloconic sensilla inhibited by some food odorants and terpenes (de Bruyne et al, 2001;Yao et al, 2005), and Drosophila trichoid sensilla inhibited by fruit odorants (Hallem et al, 2004). A survey of some Drosophila olfactory receptor molecules to a wide range of odorants found 17% excitatory versus 11% inhibitory responses .…”

A microfluidics-based method for measuring neuronal activity in Drosophila chemosensory neurons

“…The fruit fly Drosophila melanogaster is widely used as a genetic model organism to uncover basic mechanisms of taste coding and odor perception [1][2][3][4][5][6][7] . Recent insights into the molecular and functional mechanisms of sensory perception in Drosophila have been achieved by the use of single-sensillum recordings of adult taste or olfactory sensilla 1,4,[8][9][10][11][12][13] . This method enables sensitive measurements of action potential patterns and shows whether responses are excitatory or inhibitory, but drawing final conclusions about the individual firing neuron is difficult, as each sensillum contains two to four neurons 14 .…”