Chih-Ying Su

Olfactory Perception: Receptors, Cells, and Circuits

Remarkable advances in our understanding of olfactory perception have been made in recent years, including the discovery of new mechanisms of olfactory signaling and new principles of olfactory processing. Here, we discuss the insight that has been gained into the receptors, cells, and circuits that underlie the sense of smell.

Non-synaptic inhibition between grouped neurons in an olfactory circuit

Diverse sensory organs, including mammalian taste buds and insect chemosensory sensilla, show a marked compartmentalization of receptor cells; however, the functional impact of this organization remains unclear. Here we show that compartmentalized Drosophila olfactory receptor neurons (ORNs) communicate with each other directly. The sustained response of one ORN is inhibited by the transient activation of a neighbouring ORN. Mechanistically, such lateral inhibition does not depend on synapses and is probably mediated by ephaptic coupling. Moreover, lateral inhibition in the periphery can modulate olfactory behaviour. Together, the results show that integration of olfactory information can occur via lateral interactions between ORNs. Inhibition of a sustained response by a transient response may provide a means of encoding salience. Finally, a CO2-sensitive ORN in the malaria mosquito Anopheles can also be inhibited by excitation of an adjacent ORN, suggesting a broad occurrence of lateral inhibition in insects and possible applications in insect control.

Parietal-Eye Phototransduction Components and Their Potential Evolutionary Implications

The parietal-eye photoreceptor is unique because it has two antagonistic light signaling pathways in the same cell—a hyperpolarizing pathway maximally sensitive to blue light and a depolarizing pathway maximally sensitive to green light. Here, we report the molecular components of these two pathways. We found two opsins in the same cell: the blue-sensitive pinopsin and a previously unidentified green-sensitive opsin, which we name parietopsin. Signaling components included gustducin-α and Gαo, but not rod or cone transducin-α. Single-cell recordings demonstrated that Go mediates the depolarizing response. Gustducin-α resembles transducin-α functionally and likely mediates the hyperpolarizing response. The parietopsin-Go signaling pair provides clues about how rod and cone phototransduction might have evolved.

Temporal coding of odor mixtures in an olfactory receptor neuron

Most natural odors are mixtures and often elicit percepts distinct from those elicited by their constituents. This emergence of a unique odor quality has long been attributed to central processing. Here we show that sophisticated integration of olfactory information begins in olfactory receptor neurons (ORNs) in Drosophila. Odor mixtures are encoded in the temporal dynamics as well as in the magnitudes of ORN responses. ORNs can respond to an inhibitory odorant with different durations depending on the level of background excitation. ORNs respond to mixtures with distinctive temporal dynamics that reflect the physicochemical properties of the constituent odorants. The insect repellent DEET (N,N-diethyl-m-toluamide), which attenuates odor responses of multiple ORNs, differs from an ORN-specific inhibitor in its effects on temporal dynamics. Our analysis reveals a means by which integration of information from odor mixtures begins in ORNs and provides insight into the contribution of inhibitory stimuli to sensory coding.

Malaria Parasites Produce Volatile Mosquito Attractants

ABSTRACT The malaria parasite Plasmodium falciparum contains a nonphotosynthetic plastid organelle that possesses plant-like metabolic pathways. Plants use the plastidial isoprenoid biosynthesis pathway to produce volatile odorants, known as terpenes. In this work, we describe the volatile chemical profile of cultured malaria parasites. Among the identified compounds are several plant-like terpenes and terpene derivatives, including known mosquito attractants. We establish the molecular identity of the odorant receptors of the malaria mosquito vector Anopheles gambiae, which responds to these compounds. The malaria parasite produces volatile signals that are recognized by mosquitoes and may thereby mediate host attraction and facilitate transmission. IMPORTANCE Malaria is a key global health concern. Mosquitoes that transmit malaria are more attracted to malaria parasite-infected mammalian hosts. These studies aimed to understand the chemical signals produced by malaria parasites; such an understanding may lead to new transmission-blocking strategies or noninvasive malaria diagnostics. Malaria is a key global health concern. Mosquitoes that transmit malaria are more attracted to malaria parasite-infected mammalian hosts. These studies aimed to understand the chemical signals produced by malaria parasites; such an understanding may lead to new transmission-blocking strategies or noninvasive malaria diagnostics.

Circuit Logic of Avoidance and Attraction

The intensities and context of sensory stimuli are encoded by specific neural circuits that instruct behavioral responses. [Also see Reports by Zhang et al. and Lin et al.] How an animal responds to a sensory stimulus depends on its intensity. Animals prefer food with moderate concentrations of salt and avoid food high in salt content. Responses may also depend on the context. Carbon dioxide (CO2) emitted by stressed fruit flies elicits an avoidance response (1). However, CO2 emitted by fermenting fruits is tolerated by flies in the context of food odors (2). How is a sensory stimulus encoded when presented at different intensities or in different contexts? On pages 1338 and 1334 in this issue, Lin et al. (3) and Zhang et al. (4) provide new insight into this fascinating problem by investigating how different concentrations of CO2 and salt are encoded by the olfactory and gustatory systems, respectively, in the fruit fly Drosophila melanogaster.