Insect olfaction from model systems to disease control

Abstract

Great progress has been made in the field of insect olfaction in recent years. Receptors, neurons, and circuits have been defined in considerable detail, and the mechanisms by which they detect, encode, and process sensory stimuli are being unraveled. We provide a guide to recent progress in the field, with special attention to advances made in the genetic model organism Drosophila. We highlight key questions that merit additional investigation. We then present our view of how recent advances may be applied to the control of disease-carrying insects such as mosquitoes, which transmit disease to hundreds of millions of people each year. We suggest how progress in defining the basic mechanisms of insect olfaction may lead to means of disrupting host-seeking and other olfactory behaviors, thereby reducing the transmission of deadly diseases.

Fig. 1.

Insect antennae. (Clockwise from upper left) Moth (Image courtesy of Geoffrey Attardo, Yale School of Public Health); Leconte's Scarab, Chrysina lecontei (Image courtesy of Alex Wild); nymph of Barytettix humphreysi (Image courtesy of Jeffrey C. Oliver); meloid beetle, Lytta magister (Image courtesy of Jeffrey C. Oliver); butterfly (Image courtesy of Geoffrey Attardo); beetle (Image courtesy of Geoffrey Attardo); ant (Image courtesy of Alex Wild); lubber grasshopper (Image courtesy of Geoffrey Attardo); bald-faced hornet, Dolichovespula maculate (Image courtesy of Gary Alpert, CDC/Harvard University). (Center) Mesquite bug nymph, Thasus neocalifornicus (Image courtesy of Alex Wild).

Fig. 2.

Morphology of and physiological recordings from olfactory sensilla. (A) Arrow indicates a single-walled trichoid sensillum from A. gambiae. (B) A double-walled grooved peg sensillum from A. gambiae. A and B are reprinted from ref. . (C) Single-sensillum recording method. An electrode is inserted in the lymph (L) of a sensillum, an odor stimulus is delivered, and action potentials are recorded from the ORNs. AC, accessory cells; EC, epidermal cells. Reprinted with permission from ref. . (D) Physiological recording. The bar above the trace indicates the 0.5-s odor stimulus. Action potentials of large amplitude derive from one ORN in the sensillum, and action potentials of smaller amplitude derive from the other ORN. In this trace, the ORN that produces large action potentials is excited by the odor.

Fig. 3.

Olfactory system circuitry. ORNs expressing an individual odorant receptor (same color) send axons to an individual glomerulus in the antennal lobe. In the antennal lobe, the ORNs form synaptic connections with projection neurons, which send axons to Kenyon cells of the mushroom bodies and then to the lateral horn (red and blue axons), or directly to the lateral horn (green axon). ORNs also form synapses with local neurons in the antennal lobe. Reprinted from ref. with permission from Elsevier.

Fig. 4.

Odor coding by a receptor repertoire. (A) Combinatorial coding of odors by receptors of the Drosophila larva. Colored dots indicate a strong odor response, defined as ≥100 spikes/s to a 10⁻² dilution in the empty neuron system. Reprinted from ref. with permission from Elsevier. (B) Tuning curves for a narrowly tuned receptor, Or82a, and a broadly tuned receptor, Or67a. The 110 odorants are listed along the x axis according to the magnitudes of the responses that they elicit from each receptor. The odorants that elicit the strongest responses are placed near the center of the distribution, whereas those odorants eliciting weak responses are at the edges. The order of odors is different for the two receptors. Negative values represent inhibitory responses. Reprinted from ref. with permission from Elsevier.

Fig. 5.

Insect vectors of disease. (A) A. aegypti is a vector of dengue fever and yellow fever (Image courtesy of James Gathany, CDC). (B) Phlebotomus papatasi, the sandfly, is a vector of Leishmaniasis (Image courtesy of James Gathany, CDC). (C) Tsetse fly Glossina morsitans morsitans is a vector of trypanosomiasis. [Image courtesy of Geoffrey Attardo (Reprinted from the cover of PLoS Neglected Tropical Diseases, March 12, 2008, volume 2, issue 3)]. (D) C. pipiens is a vector of West Nile virus. (Image courtesy of Geoffrey Attardo).