Propagation of olfactory information in
            <i>Drosophila</i>

Root, Cory M.; Semmelhack, Julie Lee; Wong, Allen; Flores, Jorge A.; Wang, Jing W.

doi:10.1073/pnas.0704523104

Cited by 124 publications

(135 citation statements)

References 43 publications

(53 reference statements)

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“…Furthermore, because all measurements were performed on neuron populations, the polarity of individual neurons may be lost in our recordings. Therefore, single cell measurements with activity dependent proteins, ideally combined with single cell electrophysiology (Galizia and Kimmerle, 2004;Wilson et al, 2004;Root et al, 2007) would be helpful.…”

Section: Discussionmentioning

confidence: 99%

Olfactory Information Processing in theDrosophilaAntennal Lobe: Anything Goes?

Silbering¹,

Okada²,

Ito³

et al. 2008

J. Neurosci.

119

131

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When an animal smells an odor, olfactory sensory neurons generate an activity pattern across olfactory glomeruli of the first sensory neuropil, the insect antennal lobe or the vertebrate olfactory bulb. Here, several networks of local neurons interact with sensory neurons and with output neurons-insect projection neurons, or vertebrate mitral/tufted cells. The extent and form of information processing taking place in these local networks has been subject of controversy. To investigate the role of local neurons in odor information processing we have used the calcium sensor G-CaMP to perform in vivo recordings of odor-evoked spatiotemporal activity patterns in five genetically defined neuron populations of the antennal lobe of Drosophila melanogaster: three distinct populations of local neurons (two GABAergic and one cholinergic), as well as sensory neurons and projection neurons. Odor-specific and concentration dependent spatiotemporal response patterns varied among neuron populations. Activity transfer differed along the olfactory pathway for different glomerulus-odor combinations: we found cases of profile broadening and of linear and complex transfer. Moreover, the discriminability between the odors also varied across neuron populations and was maximal in projection neurons. Discriminatory power increased with higher odor concentrations over a wide dynamic range, but decreased at the highest concentration. These results show the complexity and diversity of odor information processing mechanisms across olfactory glomeruli in the fly antennal lobe.

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Section: Discussionmentioning

confidence: 99%

Olfactory Information Processing in theDrosophilaAntennal Lobe: Anything Goes?

Silbering¹,

Okada²,

Ito³

et al. 2008

J. Neurosci.

119

131

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“…Functional imaging and electrophysiological studies have provided useful insights into information processing in the antennal lobe and mushroom body (39)(40)(41)42). Although local interneurons modulate PNs activity, ORNs are the primary drivers of this activity (43). Thus, odor experience-based plasticity in ORN coding is likely to influence PN tuning and enables the animal to identify an odor and assess its concentration in different environmental contexts.…”

Section: Discussionmentioning

confidence: 99%

Post-eclosion odor experience modifies olfactory receptor neuron coding in Drosophila

Iyengar

Chakraborty

Goswami

et al. 2010

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

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Olfactory responses of Drosophila undergo pronounced changes after eclosion. The flies develop attraction to odors to which they are exposed and aversion to other odors. Behavioral adaptation is correlated with changes in the firing pattern of olfactory receptor neurons (ORNs). In this article, we present an information-theoretic analysis of the firing pattern of ORNs. Flies reared in a synthetic odorless medium were transferred after eclosion to three different media: (i) a synthetic medium relatively devoid of odor cues, (ii) synthetic medium infused with a single odorant, and (iii) complex cornmeal medium rich in odors. Recordings were made from an identified sensillum (type II), and the Jensen-Shannon divergence (D JS ) was used to assess quantitatively the differences between ensemble spike responses to different odors. Analysis shows that prolonged exposure to ethyl acetate and several related esters increases sensitivity to these esters but does not improve the ability of the fly to distinguish between them. Flies exposed to cornmeal display varied sensitivity to these odorants and at the same time develop greater capacity to distinguish between odors. Deprivation of odor experience on an odorless synthetic medium leads to a loss of both sensitivity and acuity. Rich olfactory experience thus helps to shape the ORNs response and enhances its discriminative power. The experiments presented here demonstrate an experience-dependent adaptation at the level of the receptor neuron.imaginal conditioning | sensory adaptation | odor imprinting | JensenShannon divergence | chemo receptor tuning O lfaction in the fruit fly, Drosophila melanogaster, is crucial for a variety of behaviors, including associative learning (1, 2), courtship (3), foraging (4), and flight (5, 6). Odorants are detected by approximately 1,300 olfactory receptor neurons (ORNs), which are housed in sensilla on the third antennal segment and individually express one of approximately 50 functional odor receptors in adults (7-9). All ORNs expressing the same olfactory receptor project to one of approximately 50 glomeruli in the antennal lobe, where they synapse with a set of projection neurons (PNs) (10, 11). The activity of ORNs, either excitation or inhibition, provides behaviorally relevant information about odorants such as their identity, concentration, and source. The information transduced by an ORN is processed in the antennal lobe (12, 13) and sent via PNs to the mushroom bodies, which are believed to be centers for olfactory learning and memory (14, 15).Experience-dependent modifiability (i.e., plasticity) of olfactory representation at the level of the central nervous system is well known (2,16,17). Relatively little attention has been paid to long-term changes in sensory neuron activity resulting from odor experiences. It was previously shown that exposure of newly born imago to a particular set of odorants alters their responses to these odors (18,19). The flies develop an attraction to the chemicals to which they are exposed and an av...

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“…LNs in the antennal lobe have been suggested to play a role in the transformation of olfactory information, and thus the shaping of elaborate behavioral responses to odor cues, through synaptic interactions with the ORNs and PNs in the antennal lobe circuitry (13,14,(25)(26)(27)(28)(29). Immunocytochemistry with a well characterized antiserum has revealed that DTKs are expressed in certain LNs that form a dense supply of neuronal processes to the antennal lobe glomeruli (21).…”

Section: Distribution Of Dtk Peptide and Its Receptor Dtkr In The Olfmentioning

confidence: 99%

Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila

Ignell

Root

Birse

et al. 2009

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

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161

197

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The role of classical neurotransmitters in the transfer and processing of olfactory information is well established in many organisms. Neuropeptide action, however, is largely unexplored in any peripheral olfactory system. A subpopulation of local interneurons (LNs) in the Drosophila antannal lobe is peptidergic, expressing Drosophila tachykinins (DTKs). We show here that olfactory receptor neurons (ORNs) express the DTK receptor (DTKR). Using twophoton microscopy, we found that DTK applied to the antennal lobe suppresses presynaptic calcium and synaptic transmission in the ORNs. Furthermore, reduction of DTKR expression in ORNs by targeted RNA interference eliminates presynaptic suppression and alters olfactory behaviors. We detect opposite behavioral phenotypes after reduction and over expression of DTKR in ORNs. Our findings suggest a presynaptic inhibitory feedback to ORNs from peptidergic LNs in the antennal lobe.olfactory behavior ͉ presynaptic inhibition ͉ tachykinin ͉ two-photon imaging I n Drosophila, odor detection begins when odor molecules activate olfactory receptor neurons (ORNs) in the antennae and maxillary palps. Each of the ORNs expresses only 1 or a few members of a large family of odorant receptor genes (1-4). These ORNs propagate activity to neurons with dendrites in the glomerular compartments of the antennal lobe; each glomerulus receives inputs from ORNs that express the same odorant receptor (1, 3, 5, 6). In the glomeruli, the activity is read by second-order neurons, designated projection neurons (PNs), which relay information to higher olfactory centers in the brain (7).Inhibitory circuits in the glomeruli, mediated by local interneurons (LNs), play a key role in modulating glomerular signal activity. Presynaptic GABAergic inhibition of the ORNs has been shown in both Drosophila (8, 9) and in mammals (10-12). Conversely, cholinergic LNs in the Drosophila antennal lobe have been suggested to increase and redistribute odor-evoked activity at low odor concentrations (13,14).In addition to GABA and acetylcholine it is likely that certain neuropeptides are used as neuromodulators in the antennal lobe circuitry of insects (15, 16), as also suggested in the olfactory bulb in mammals (17,18). One neuropeptide gene that has been implicated in olfactory processing is dtk (19), a gene encoding 5 tachykinin-related peptides, DTKs (20). The DTKs are expressed in Ϸ150 neurons in the Drosophila brain, and in the antennal lobe glomeruli, there are extensive DTK-immunoreactive arborizations derived from a subset of antennal lobe LNs (21). Two DTK receptors, DTKR and NKD, have been identified in Drosophila (22, 23) and 1 of these, DTKR, is strongly expressed in antennal lobe glomeruli (24). Behavioral evidence for a role of DTKs in olfaction was obtained from analysis of flies where dtk expression was knocked down globally using RNA interference (RNAi); these flies displayed diminished odor sensitivity (19).To gain insight into the neuromodulation provided by the DTK signaling system in the antennal lob...

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Propagation of olfactory information in Drosophila

Cited by 124 publications

References 43 publications

Olfactory Information Processing in theDrosophilaAntennal Lobe: Anything Goes?

Olfactory Information Processing in theDrosophilaAntennal Lobe: Anything Goes?

Post-eclosion odor experience modifies olfactory receptor neuron coding in Drosophila

Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila

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