Translation of Sensory Input into Behavioral Output via an Olfactory System

Kreher, Scott A.; Mathew, Dennis; Kim, Junhyong; Carlson, John R.

doi:10.1016/j.neuron.2008.06.010

Cited by 257 publications

(465 citation statements)

References 59 publications

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“…We wished to determine whether, for each ORN of the larval olfactory system, we could identify an odorant that excited the neuron strongly, and, if so, whether it activated the neuron selectively. Toward this end, we examined the 21 larval Ors that were previously found to be functional in the empty neuron system (5)(6)(7)(8). In this system, individual Ors are expressed in a mutant neuron of the adult antenna that lacks an endogenous functional Or (8,13).…”

Section: Resultsmentioning

confidence: 99%

“…Toward this end, we examined the 21 larval Ors that were previously found to be functional in the empty neuron system (5)(6)(7)(8). In this system, individual Ors are expressed in a mutant neuron of the adult antenna that lacks an endogenous functional Or (8,13). Odorant responses conferred by the ectopic expression of Ors correspond well to the activities of the ORN in which the receptor is endogenously expressed in a variety of cases,…”

Section: Resultsmentioning

confidence: 99%

“…The analysis provides a foundation for elucidating the circuitry that translates receptor responses into behavior. including receptors of Drosophila adults (13,17) and larvae (8), and of mosquitoes (18).…”

Section: Significancementioning

confidence: 99%

“…ORNs together express 25 members of the Or family of odor receptors and the Orco coreceptor (5)(6)(7)(8). In each ORN, an Or and Orco together form a ligand-gated ion channel (9)(10)(11).…”

mentioning

confidence: 99%

“…The responses of the larval Or repertoire to a limited odorant panel was previously examined in an in vivo expression system known as the empty neuron system (8,13). With the use of this system, 21 of the larval Ors were found to be functional.…”

mentioning

confidence: 99%

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Functional diversity among sensory receptors in a Drosophila olfactory circuit

Mathew

Martelli

Kelley-Swift

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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The ability of an animal to detect, discriminate, and respond to odors depends on the function of its olfactory receptor neurons (ORNs), which in turn depends ultimately on odorant receptors. To understand the diverse mechanisms used by an animal in olfactory coding and computation, it is essential to understand the functional diversity of its odor receptors. The larval olfactory system of Drosophila melanogaster contains 21 ORNs and a comparable number of odorant receptors whose properties have been examined in only a limited way. We systematically screened them with a panel of ∼500 odorants, yielding >10,000 receptor-odorant combinations. We identify for each of 19 receptors an odorant that excites it strongly. The responses elicited by each of these odorants are analyzed in detail. The odorants elicited little cross-activation of other receptors at the test concentration; thus, low concentrations of many of these odorants in nature may be signaled by a single ORN. The receptors differed dramatically in sensitivity to their cognate odorants. The responses showed diverse temporal dynamics, with some odorants eliciting supersustained responses. An intriguing question in the field concerns the roles of different ORNs and receptors in driving behavior. We found that the cognate odorants elicited behavioral responses that varied across a broad range. Some odorants elicited strong physiological responses but weak behavioral responses or weak physiological responses but strong behavioral responses.T he olfactory system of the Drosophila larva achieves remarkable function with minimal structure. It detects and responds to spatial and temporal gradients of odorants, transforming chemical information into navigation via an elegant repertoire of head sweeps, runs, and turns (1-3). Its sophisticated function is based on the activities of 21 olfactory receptor neurons (ORNs), which innervate the dorsal organ of the head and send axons to the antennal lobe of the brain (4). The activities of the ORNs are in turn based on the responses of odor receptors (Ors). Thus, to understand the molecular basis of larval olfactory navigation, it is necessary to understand the function of the receptors.ORNs together express 25 members of the Or family of odor receptors and the Orco coreceptor (5-8). In each ORN, an Or and Orco together form a ligand-gated ion channel (9-11). Most ORNs express a single Or, although one ORN coexpresses Or94a and Or94b and another ORN coexpresses Or33b and Or47a (7). The significance of this coexpression remains speculative, but the response profiles of some coexpressed adult Ors are additive (12).The responses of the larval Or repertoire to a limited odorant panel was previously examined in an in vivo expression system known as the empty neuron system (8, 13). With the use of this system, 21 of the larval Ors were found to be functional. However, studies of the larval Or repertoire have been limited not only in the number of odorants examined, but also in their consideration of receptor sensitivity, tempor...

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Significancementioning

confidence: 99%

“…ORNs together express 25 members of the Or family of odor receptors and the Orco coreceptor (5)(6)(7)(8). In each ORN, an Or and Orco together form a ligand-gated ion channel (9)(10)(11).…”

mentioning

confidence: 99%

mentioning

confidence: 99%

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Functional diversity among sensory receptors in a Drosophila olfactory circuit

Mathew

Martelli

Kelley-Swift

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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107

184

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Diversity, variability, and suboesophageal connectivity of antennal lobe neurons in D. melanogaster larvae

Thum

Leisibach

Gendre

et al. 2011

J of Comparative Neurology

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Whereas the ''vertical'' elements of the insect olfactory pathway, the olfactory receptor neurons and the projection neurons, have been studied in great detail, local interneurons providing ''horizontal'' connections in the antennal lobe were ignored for a long time. Recent studies in adult Drosophila demonstrate diverse roles for these neurons in the integration of odor information, consistent with the identification of a large variety of anatomical and neurochemical subtypes. Here we focus on the larval olfactory circuit of Drosophila, which is much reduced in terms of cell numbers. We show that the horizontal connectivity in the larval antennal lobe differs largely from its adult counterpart. Only one of the five anatomical types of neurons we describe is restricted to the antennal lobe and therefore fits the definition of a local interneuron. Interestingly, the four remaining subtypes innervate both the antennal lobe and the suboesophageal ganglion. In the latter, they may overlap with primary gustatory terminals and with arborizations of hugin cells, which are involved in feeding control. This circuitry suggests special links between smell and taste, which may reflect the chemosensory constraints of a crawling and burrowing lifestyle. We also demonstrate that many of the neurons we describe exhibit highly variable trajectories and arborizations, especially in the suboesophageal ganglion. Together with reports from adult Drosophila, these data suggest that wiring variability may be another principle of insect brain organization, in parallel with stereotypy.

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Dissecting the molecular mechanism of drosophila odorant receptors through activity modeling and comparative analysis

Guo

Kim

2009

Proteins

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To gain insight into the molecular mechanism of odorant receptors (ORs) in Drosophila species, we developed a Quantitative Structure Activity Relationship (QSAR) model that predicts experimentally measured electrophysiological activities between 24 D. melanogaster ORs and 108 odorants. Although the model is limited by the tested odorants,analyzing the model allowed dissection of specific topological and chemical properties necessary for an odorant to elicit excitatory or inhibitory receptor response. Linear odorants with five to eight nonhydrogen atoms at the main chain and hydrogen-bond acceptor and/or hydrogen-bond donor at its ends were found to stimulate strong excitatory response. A comparative sequence analysis of 90 ORs in 15 orthologous groups identified 15 putative specificity-determining residues (SDRs) and 15 globally conserved residues that we postulate as functionally key residues. Mapping to a model of secondary structure resulted in 14 out of 30 key residues locating to the transmembrane (TM) domains. Twelve residues, including six SDRs and six conserved residues, are located at the extracellular halves of the TM domains. Combining the evidence from the QSAR modeling and the comparative sequence analysis, we hypothesize that the Drosophila ORs accept odorants into a binding pocket located on the extracellular halves of its TM domains. The QSAR modeling suggests that the binding pocket is around 15 A in depth and about 6 A in width. Twelve mainly polar or charged key residues, both SDRs and conserved, are located in this pocket and postulated to distinguish docked odorants via primarily geometry fitting and hydrogen-bond interaction.

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Translation of Sensory Input into Behavioral Output via an Olfactory System

Cited by 257 publications

References 59 publications

Functional diversity among sensory receptors in a Drosophila olfactory circuit

Functional diversity among sensory receptors in a Drosophila olfactory circuit

Diversity, variability, and suboesophageal connectivity of antennal lobe neurons in D. melanogaster larvae

Dissecting the molecular mechanism of drosophila odorant receptors through activity modeling and comparative analysis

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