Complementary Function and Integrated Wiring of the Evolutionarily Distinct<i>Drosophila</i>Olfactory Subsystems

Silbering, Ana F.; Rytz, Raphael; Grosjean, Yaël; Abuin, Liliane; Ramdya, Pavan; Jefferis, Gregory S.X.E.; Benton, Richard

doi:10.1523/jneurosci.2360-11.2011

Cited by 464 publications

(809 citation statements)

References 119 publications

(256 reference statements)

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“…Thus, we were able to record a subpopulation of Ir-expressing OSNs with a distinct odor spectrum (Fig. 3A) similar to that of ac3A neurons (16,32). When stimulated with butyric acid, the OSN fired bursts of action potentials, with increasing firing frequency at higher odor concentrations (Fig.…”

Section: Patch-clamp Recordings Of Odor Responses In Or-expressing Osnsmentioning

confidence: 82%

“…To date, Drosophila is the only model organism for which odor selectivity is known for most of its odorant receptors (Ors) (10,11), and an Or expression pattern has been mapped to OSNs (12,13). In addition, another family of chemoreceptors called ionotropic receptors (Irs) has been identified and characterized (14)(15)(16). These two types of chemoreceptors respond to different odors, thus endowing Drosophila OSNs with unique and complementary properties for odor detection (17).…”

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confidence: 99%

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Distinct signaling of Drosophila chemoreceptors in olfactory sensory neurons

Cao

Jing

Yang

et al. 2016

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

114

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In Drosophila, olfactory sensory neurons (OSNs) rely primarily on two types of chemoreceptors, odorant receptors (Ors) and ionotropic receptors (Irs), to convert odor stimuli into neural activity. The cellular signaling of these receptors in their native OSNs remains unclear because of the difficulty of obtaining intracellular recordings from Drosophila OSNs. Here, we developed an antennal preparation that enabled the first recordings (to our knowledge) from targeted Drosophila OSNs through a patch-clamp technique. We found that brief odor pulses triggered graded inward receptor currents with distinct response kinetics and current-voltage relationships between Or-and Ir-driven responses. When stimulated with long-step odors, the receptor current of Ir-expressing OSNs did not adapt. In contrast, Or-expressing OSNs showed a strong Ca 2+ -dependent adaptation. The adaptation-induced changes in odor sensitivity obeyed the Weber-Fechner relation; however, surprisingly, the incremental sensitivity was reduced at low odor backgrounds but increased at high odor backgrounds. Our model for odor adaptation revealed two opposing effects of adaptation, desensitization and prevention of saturation, in dynamically adjusting odor sensitivity and extending the sensory operating range.Drosophila | olfaction | chemoreceptor | sensory adaptation | OSN

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Section: Patch-clamp Recordings Of Odor Responses In Or-expressing Osnsmentioning

confidence: 82%

mentioning

confidence: 99%

Distinct signaling of Drosophila chemoreceptors in olfactory sensory neurons

Cao

Jing

Yang

et al. 2016

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

114

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“…These receptors are present in a distinct class of sensilla (coeloconic), tend to respond to acids and amines, and are related to the family of ionotropic glutamate receptors present at synapses. The IRs project to distinct glomeruli in the antennal lobe, and from there to Kenyon cells, but the responses of individual IR types to a panel of odors is, as yet, unknown (17), so the IRs responses cannot be related to the OR responses described here.…”

Section: Discussionmentioning

confidence: 93%

A statistical property of fly odor responses is conserved across odors

Stevens

2016

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

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I have reanalyzed the data presented by Hallem and Carlson [Hallem EA, Carlson JR (2006) Cell 125(1):143-160] and shown that the combinatorial odor code supplied by the fruit fly antenna is a very simple one in which nearly all odors produce, statistically, the same neuronal response; i.e., the probability distribution of sensory neuron firing rates across the population of odorant sensory neurons is an exponential for nearly all odors and odor mixtures, with the mean rate dependent on the odor concentration. Between odors, then, the response differs according to which sensory neurons are firing at what individual rates and with what mean population rate, but not in the probability distribution of firing rates. This conclusion is independent of adjustable parameters, and holds both for monomolecular odors and complex mixtures. Because the circuitry in the antennal lobe constrains the mean firing rate to be the same for all odors and concentrations, the odor code is what is known as maximum entropy.fly | olfaction | theory | odor code T he projection neurons of the fly antennal lobe present odor information to the Kenyon cells of the mushroom body in the form of a combinatorial code-each odor is specified by a particular pattern of firing rates across the population of projection neurons-and a recent paper (1), using data published in ref. 2, provided preliminary evidence that this odor code is what information theorists call maximum entropy (3). To understand what a maximum entropy code is, suppose that we record the firing rates from, say, 10 different projection neurons, each presented with, say, 10 different odors to give a total of 100 firing rates. Now make a histogram of these firing rates. If the odor code is maximum entropy, this histogram would have nearly the same shape no matter which projection neurons and which odors were chosen. Also, the larger the sample of projection neurons and/or odors, the closer the shapes of histograms would be. Remarkably, if only a single odor and many projection neurons, or a single projection neuron and many odors, are used to generate the rates, the histogram shape is always nearly the same.Many different maximum entropy codes have been studied, and the type of code is defined by the shape of the histogram that results from a sample of rates. The histogram in each case is an approximation of a probability distribution of rates. For example, if the mean rate is always the same, the maximum entropy code is known to be associated with an exponential distribution of rates, and if both the mean and variance are always the same, a Gaussian distribution of rates is associated (3). For the fly projection neurons, the associated probability distribution of rates is proposed to be an exponential (1) (with always the same mean).As pointed out earlier (1), a maximum entropy code would be advantageous to the fly because it would permit the most odors to be discriminated with the available number of odorant receptors.This characterization of the odor code used by antennal lobe proje...

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“…In the visual and auditory systems, neighboring neurons in the input field target the neighboring regions in the output field (Flanagan 2006;Kandler et al 2009). In the olfactory systems of mammals and insects, the axons of the primary olfactory receptor neurons (ORNs) that express the same olfactory or ionotropic receptors converge to one specific glomerulus in the primary olfactory center (Couto et al 2005;Sakano 2010;Silbering et al 2011). The ORN axons form synaptic connections with dendrites of second-order neurons that also typically target one particular glomerulus among those discretely distributed.…”

mentioning

confidence: 99%

Dendritic Eph organizes dendrodendritic segregation in discrete olfactory map formation in Drosophila

Anzo¹,

Sekine²,

Makihara³

et al. 2017

Genes Dev.

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Proper function of the neural network results from the precise connections between axons and dendrites of presynaptic and postsynaptic neurons, respectively. In the Drosophila olfactory system, the dendrites of projection neurons (PNs) stereotypically target one of ∼50 glomeruli in the antennal lobe (AL), the primary olfactory center in the brain, and form synapses with the axons of olfactory receptor neurons (ORNs). Here, we show that Eph and Ephrin, the well-known axon guidance molecules, instruct the dendrodendritic segregation during the discrete olfactory map formation. The Eph receptor tyrosine kinase is highly expressed and localized in the glomeruli related to reproductive behavior in the developing AL. In one of the pheromone-sensing glomeruli (DA1), the Eph cell-autonomously regulates its dendrites to reside in a single glomerulus by interacting with Ephrins expressed in adjacent PN dendrites. Our data demonstrate that the trans interaction between dendritic Eph and Ephrin is essential for the PN dendritic boundary formation in the DA1 olfactory circuit, potentially enabling strict segregation of odor detection between pheromones and the other odors.

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Complementary Function and Integrated Wiring of the Evolutionarily DistinctDrosophilaOlfactory Subsystems

Cited by 464 publications

References 119 publications

Distinct signaling of Drosophila chemoreceptors in olfactory sensory neurons

Distinct signaling of Drosophila chemoreceptors in olfactory sensory neurons

A statistical property of fly odor responses is conserved across odors

Dendritic Eph organizes dendrodendritic segregation in discrete olfactory map formation in Drosophila

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