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Decoding odor quality and intensity in the Drosophila brain.

Strutz A, Soelter J, Baschwitz A, Farhan A, Grabe V, Rybak J, Knaden M, Schmuker M, Hansson BS, Sachse S - Elife (2014)

Bottom Line: Silencing iPNs severely diminished flies' attraction behavior.Moreover, functional imaging disclosed a LH region tuned to repulsive odors comprised exclusively of third-order neurons.We provide evidence for a feature-based map in the LH, and elucidate its role as the center for integrating behaviorally relevant olfactory information.

View Article: PubMed Central - PubMed

Affiliation: Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Jena, Germany.

ABSTRACT
To internally reflect the sensory environment, animals create neural maps encoding the external stimulus space. From that primary neural code relevant information has to be extracted for accurate navigation. We analyzed how different odor features such as hedonic valence and intensity are functionally integrated in the lateral horn (LH) of the vinegar fly, Drosophila melanogaster. We characterized an olfactory-processing pathway, comprised of inhibitory projection neurons (iPNs) that target the LH exclusively, at morphological, functional and behavioral levels. We demonstrate that iPNs are subdivided into two morphological groups encoding positive hedonic valence or intensity information and conveying these features into separate domains in the LH. Silencing iPNs severely diminished flies' attraction behavior. Moreover, functional imaging disclosed a LH region tuned to repulsive odors comprised exclusively of third-order neurons. We provide evidence for a feature-based map in the LH, and elucidate its role as the center for integrating behaviorally relevant olfactory information.

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Characterization of excitatory and inhibitory projection neurons.Overlap of ePNs (QUAS-tdTomato) and iPNs (UAS-GCaMP3.0) in the LH area. The circle indicates the posterior lateral region, which is sparsely innervated by iPNs and dominated by ePN axonal terminal fields. Scale bar, 20 µm.DOI:http://dx.doi.org/10.7554/eLife.04147.004
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fig1s1: Characterization of excitatory and inhibitory projection neurons.Overlap of ePNs (QUAS-tdTomato) and iPNs (UAS-GCaMP3.0) in the LH area. The circle indicates the posterior lateral region, which is sparsely innervated by iPNs and dominated by ePN axonal terminal fields. Scale bar, 20 µm.DOI:http://dx.doi.org/10.7554/eLife.04147.004

Mentions: Cell bodies of iPNs are exclusively located in the ventral cell cluster which consists of ∼50 iPNs (Lai et al., 2008) that project via the mACT to the LH, thereby bypassing the MBc (Ito et al., 1997) (Figure 1A,B). In contrast, ePN somata are located anterodorsally and laterally of the AL, and their axons project through the iACT or oACT to the MBc and the LH (Stocker et al., 1997; Marin et al., 2002; Wong et al., 2002; Lai et al., 2008). To analyze the innervation patterns of iPNs and ePNs, we labeled both PN populations simultaneously in vivo using the enhancer trap lines GH146-QF and MZ699-GAL4 that label the majority of ePNs (60%) and iPNs (86%), respectively (Lai et al., 2008). Double-labeling shows that both PN types innervate overlapping regions in the AL and the LH, while a small posterior-lateral LH area is targeted only by ePNs (Figure 1A, Figure 1—figure supplement 1). In GH146-positive (GH146+) PNs, immunolabeling reveals GABA production in all ∼6 PNs of the ventral cell cluster (Wilson and Laurent, 2005), whereas ePNs of this line are exclusively cholinergic (Shang et al., 2007). For the ∼45 MZ699-positive (MZ699+) iPNs (Lai et al., 2008), GAD1 (glutamic acid decarboxylase) in situ hybridizations imply GABA synthesis (Okada et al., 2009), which was recently verified via immunostaining (Liang et al., 2013; Parnas et al., 2013). The polarity of both PN populations has been studied in detail, showing that both possess dendritic regions in the AL, indicating the AL as their cholinergic input site, while the LH represents their major output site (Jefferis et al., 2001; Okada et al., 2009; Liang et al., 2013; Parnas et al., 2013).10.7554/eLife.04147.003Figure 1.Detailed glomerular innervations of excitatory and inhibitory projection neurons in the AL.


Decoding odor quality and intensity in the Drosophila brain.

Strutz A, Soelter J, Baschwitz A, Farhan A, Grabe V, Rybak J, Knaden M, Schmuker M, Hansson BS, Sachse S - Elife (2014)

Characterization of excitatory and inhibitory projection neurons.Overlap of ePNs (QUAS-tdTomato) and iPNs (UAS-GCaMP3.0) in the LH area. The circle indicates the posterior lateral region, which is sparsely innervated by iPNs and dominated by ePN axonal terminal fields. Scale bar, 20 µm.DOI:http://dx.doi.org/10.7554/eLife.04147.004
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4270039&req=5

fig1s1: Characterization of excitatory and inhibitory projection neurons.Overlap of ePNs (QUAS-tdTomato) and iPNs (UAS-GCaMP3.0) in the LH area. The circle indicates the posterior lateral region, which is sparsely innervated by iPNs and dominated by ePN axonal terminal fields. Scale bar, 20 µm.DOI:http://dx.doi.org/10.7554/eLife.04147.004
Mentions: Cell bodies of iPNs are exclusively located in the ventral cell cluster which consists of ∼50 iPNs (Lai et al., 2008) that project via the mACT to the LH, thereby bypassing the MBc (Ito et al., 1997) (Figure 1A,B). In contrast, ePN somata are located anterodorsally and laterally of the AL, and their axons project through the iACT or oACT to the MBc and the LH (Stocker et al., 1997; Marin et al., 2002; Wong et al., 2002; Lai et al., 2008). To analyze the innervation patterns of iPNs and ePNs, we labeled both PN populations simultaneously in vivo using the enhancer trap lines GH146-QF and MZ699-GAL4 that label the majority of ePNs (60%) and iPNs (86%), respectively (Lai et al., 2008). Double-labeling shows that both PN types innervate overlapping regions in the AL and the LH, while a small posterior-lateral LH area is targeted only by ePNs (Figure 1A, Figure 1—figure supplement 1). In GH146-positive (GH146+) PNs, immunolabeling reveals GABA production in all ∼6 PNs of the ventral cell cluster (Wilson and Laurent, 2005), whereas ePNs of this line are exclusively cholinergic (Shang et al., 2007). For the ∼45 MZ699-positive (MZ699+) iPNs (Lai et al., 2008), GAD1 (glutamic acid decarboxylase) in situ hybridizations imply GABA synthesis (Okada et al., 2009), which was recently verified via immunostaining (Liang et al., 2013; Parnas et al., 2013). The polarity of both PN populations has been studied in detail, showing that both possess dendritic regions in the AL, indicating the AL as their cholinergic input site, while the LH represents their major output site (Jefferis et al., 2001; Okada et al., 2009; Liang et al., 2013; Parnas et al., 2013).10.7554/eLife.04147.003Figure 1.Detailed glomerular innervations of excitatory and inhibitory projection neurons in the AL.

Bottom Line: Silencing iPNs severely diminished flies' attraction behavior.Moreover, functional imaging disclosed a LH region tuned to repulsive odors comprised exclusively of third-order neurons.We provide evidence for a feature-based map in the LH, and elucidate its role as the center for integrating behaviorally relevant olfactory information.

View Article: PubMed Central - PubMed

Affiliation: Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Jena, Germany.

ABSTRACT
To internally reflect the sensory environment, animals create neural maps encoding the external stimulus space. From that primary neural code relevant information has to be extracted for accurate navigation. We analyzed how different odor features such as hedonic valence and intensity are functionally integrated in the lateral horn (LH) of the vinegar fly, Drosophila melanogaster. We characterized an olfactory-processing pathway, comprised of inhibitory projection neurons (iPNs) that target the LH exclusively, at morphological, functional and behavioral levels. We demonstrate that iPNs are subdivided into two morphological groups encoding positive hedonic valence or intensity information and conveying these features into separate domains in the LH. Silencing iPNs severely diminished flies' attraction behavior. Moreover, functional imaging disclosed a LH region tuned to repulsive odors comprised exclusively of third-order neurons. We provide evidence for a feature-based map in the LH, and elucidate its role as the center for integrating behaviorally relevant olfactory information.

Show MeSH