Excitatory Interactions between Olfactory Processing Channels in the Drosophila Antennal Lobe

Olsen, Shawn R.; Bhandawat, Vikas; Wilson, Rachel I.

doi:10.1016/j.neuron.2007.03.010

Cited by 259 publications

(245 citation statements)

References 44 publications

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“…The relationship between PN local synaptic release in the antennal lobe and PN spike activity remains to be determined. While this work was in review, another paper investigating the role of lateral connections in the antennal lobe was published (31). The findings of Olsen et al (31) are qualitatively similar to ours, in that PN output is dramatically reduced in the absence of direct ORN input.…”

Section: Discussionsupporting

confidence: 79%

Propagation of olfactory information in Drosophila

Root

Semmelhack

Wong

et al. 2007

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

124

120

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Investigating how information propagates between layers in the olfactory system is an important step toward understanding the olfactory code. Each glomerular output projection neuron (PN) receives two sources of input: the olfactory receptor neurons (ORNs) of the same glomerulus and interneurons that innervate many glomeruli. We therefore asked how these inputs interact to produce PN output. We used receptor gene mutations to silence all of the ORNs innervating a specific glomerulus and recorded PN activity with two-photon calcium imaging and electrophysiology. We found evidence for balanced excitatory and inhibitory synaptic inputs but saw little or no response in the absence of direct ORN input. We next asked whether any transformation of activity occurs at successive layers of the antennal lobe. We found a strong link between PN firing and dendritic calcium elevation, the latter of which is tightly correlated with calcium activity in ORN axons, supporting the idea of glomerular propagation of olfactory information. Finally, we showed that odors are represented by a sparse population of PNs. Together, these results are consistent with the idea that direct receptor input provides the main excitatory drive to PNs, whereas interneurons modulate PN output. Balanced excitatory and inhibitory interneuron input may provide a mechanism to adjust PN sensitivity.antennal lobe ͉ gain modulation ͉ olfaction ͉ smell ͉ sparse code S ensory systems have the difficult task of encoding the identity and intensity of behaviorally relevant stimuli in the environment. The question of how these stimuli are encoded and propagated from the periphery to higher brain centers is central to systems neuroscience. The stereotypic organization of the Drosophila olfactory system and the identification of the odorant receptor genes make the fly an attractive model system in which to study the successive processing of sensory information.Drosophila olfactory receptor neurons (ORNs) in the antennae detect odors and relay neural activity to the antennal lobe in the brain. An adult fly expresses Ϸ50 odorant receptor genes (1-6). In the antennal lobe, axons of ORNs expressing the same receptor gene project with precision to spatially invariant glomeruli (4-7). Most second-order projection neurons (PNs) send dendrites to individual glomeruli in the antennal lobe and send axons to the mushroom body and the lateral horn of the protocerebrum (8-11).Imaging experiments in the insect antennal lobe (12-14) reveal a spatial map of glomerular activity. It has been hypothesized that each glomerulus is a functional unit and that the pattern of glomerular activity encodes the quality of odors (15). However, the Drosophila antennal lobe contains many GABAergic inhibitory interneurons (10,16,17), as well as a group of recently identified cholinergic excitatory interneurons (18). These two classes of interneurons apparently have opposing effects on PNs, and the extent to which they contribute to PN output is unknown. There are two general models for the function...

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Section: Discussionsupporting

confidence: 79%

Propagation of olfactory information in Drosophila

Root

Semmelhack

Wong

et al. 2007

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

124

120

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“…We then genetically engineered flies where only one type of ORN is functional, and recorded from PNs postsynaptic to silent ORNs (see the figure, panel D) in order to map the pattern of connections from the functional receptors onto other glomeruli. This experiment showed that lateral excitatory connections are spatially widespread, heterogeneous in strength, and obey connectivity rules that are stereotyped across flies (10). At about the same time, another group independently discovered a new class of cholinergic local neurons in the fly antennal lobe (11), suggesting a possible cellular substrate for the excitatory connections we had found.…”

Section: Neural Circuits Underlyingmentioning

confidence: 71%

Neural Circuits Underlying Chemical Perception

Wilson

2007

Science

Self Cite

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“…Furthermore, recent work in Drosophila has also discovered excitatory local neurons Olsen et al (2007) that form gap junctions within the AL Huang et al (2010); Yaksi and Wilson (2010). In the model presented here we only model multi-glomerular inhibitory LNs which are assumed to form GABA A synapses throughout the entire AL.…”

Section: Network Modelmentioning

confidence: 99%

“…We will here assume the same connectivity pattern for the bee. Within the AL, a network of intraand inter-glomerular inhibitory local neurons (LNs) and excitatory local neurons has been found to be involved in odour processing in the fly (Olsen et al, 2007;Shang et al, 2007;Silbering and Galizia, 2007;Silbering et al, 2008) and the bee (Sachse and Galizia, 2002). It is however currently unknown how the AL network contributes to odour segregation based on millisecond stimulus onset-asynchrony.…”

Section: Introductionmentioning

confidence: 99%

Data-driven honeybee antennal lobe model suggests how stimulus-onset asynchrony can aid odour segregation

et al. 2013

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Data-driven honeybee antennal lobe model suggests how stimulus-onset asynchrony can aid odour segregation Article (Unspecified) http://sro.sussex.ac.uk Nowotny, Thomas, Stierle, Jacob S, Galizia, C Giovanni and Szyszka, Paul (2013) Data-driven honeybee antennal lobe model suggests how stimulus-onset asynchrony can aid odour segregation. Brain Research, 1536. pp. 119-134. ISSN 0006-8993 This version is available from Sussex Research Online: http://sro.sussex.ac.uk/47660/ This document is made available in accordance with publisher policies and may differ from the published version or from the version of record. If you wish to cite this item you are advised to consult the publisher's version. Please see the URL above for details on accessing the published version. Copyright and reuse:Sussex Research Online is a digital repository of the research output of the University.Copyright and all moral rights to the version of the paper presented here belong to the individual author(s) and/or other copyright owners. To the extent reasonable and practicable, the material made available in SRO has been checked for eligibility before being made available.Copies of full text items generally can be reproduced, displayed or performed and given to third parties in any format or medium for personal research or study, educational, or not-for-profit purposes without prior permission or charge, provided that the authors, title and full bibliographic details are credited, a hyperlink and/or URL is given for the original metadata page and the content is not changed in any way. AbstractInsects have a remarkable ability to identify and track odour sources in multi-odour backgrounds. Recent behavioural experiments show that this ability relies on detecting millisecond stimulus asynchronies between odourants that originate from different sources. Honeybees, Apis mellifera, are able to distinguish mixtures where both odourants arrive at the same time (synchronous mixtures) from those where odourant onsets are staggered (asynchronous mixtures) down to an onset delay of only 6 ms. In this paper we explore this surprising ability in a model of the insects' primary olfactory brain area, the antennal lobe. We hypothesise that a winner-take-all inhibitory network of local neurons in the antennal lobe has a symmetrybreaking effect, such that the response pattern in projection neurons to an asynchronous mixture is different from the response pattern to the corresponding synchronous mixture for an extended period of time beyond the initial odourant onset where the two mixture conditions actually differ. The prolonged difference between response patterns to synchronous and asynchronous mixtures could facilitate odour segregation in downstream circuits of the olfactory pathway. We present a detailed data-driven model of the bee antennal lobe that reproduces a large data set of experimentally observed physiological odour responses, successfully implements the hypothesised symmetry-breaking mechanism and so demonstrates that this mechanism is con...

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Excitatory Interactions between Olfactory Processing Channels in the Drosophila Antennal Lobe

Cited by 259 publications

References 44 publications

Propagation of olfactory information in Drosophila

Propagation of olfactory information in Drosophila

Neural Circuits Underlying Chemical Perception

Data-driven honeybee antennal lobe model suggests how stimulus-onset asynchrony can aid odour segregation

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