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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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iPNs can be morphologically segregated according to their target and input region.(A) Principal component analysis based on the distances of the similarity scores of all terminal points of each individual iPN in the LH (for details see ‘Materials and methods’). LH-AM iPNs (blue) and LH-PM iPNs (green) form significantly distinct clusters (***p < 0.001, One-Way ANOSIM, Bray–Curtis). (B) Principal component analysis based on the glomerular innervations of each individual iPN in the AL. Again, LH-AM iPNs (blue) and LH-PM iPNs (green) form significantly distinct clusters (***p < 0.001, One-Way ANOSIM, Bray–Curtis).DOI:http://dx.doi.org/10.7554/eLife.04147.011
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fig3s1: iPNs can be morphologically segregated according to their target and input region.(A) Principal component analysis based on the distances of the similarity scores of all terminal points of each individual iPN in the LH (for details see ‘Materials and methods’). LH-AM iPNs (blue) and LH-PM iPNs (green) form significantly distinct clusters (***p < 0.001, One-Way ANOSIM, Bray–Curtis). (B) Principal component analysis based on the glomerular innervations of each individual iPN in the AL. Again, LH-AM iPNs (blue) and LH-PM iPNs (green) form significantly distinct clusters (***p < 0.001, One-Way ANOSIM, Bray–Curtis).DOI:http://dx.doi.org/10.7554/eLife.04147.011

Mentions: We next investigated if the spatially regionalized odor-evoked response patterns are reflected in the axonal terminal fields of MZ699+ iPNs in the LH. To analyze these neurons at the single neuron level, we performed neural tracing by employing a genetically encoded photoactivatable GFP (PA-GFP) (Patterson and Lippincott-Schwartz, 2002; Datta et al., 2008; Ruta et al., 2010). The photoconversion of all MZ699+ neurons leaving the AL confirmed the homogeneous distribution of iPN neurites in the LH and the sparse innervation of the posterior-lateral region as mentioned above (Figure 3A). Next we illuminated PA-GFP in single somata to selectively label individual MZ699+ iPNs from the soma up to the farthest axonal terminals in the LH. Individual iPNs were reconstructed and transformed into a reference brain using the END1-2 background (Grabe et al., 2014) to align neurons of different individuals. Based on their innervation pattern in the LH, MZ699+ iPNs could be assigned to two major morphological classes (Figure 3B,C). As expected from the extracted ORDs, one iPN group diverged to the LH-PM region (8/25 of iPNs), while a second group extended their axonal terminations within the LH-AM area (10/25 of iPNs). In order to statistically substantiate our observation, we performed a cluster analysis based on a similarity score (Kohl et al., 2013) of the target areas of all terminals of each iPN in the LH (for details see ‘Materials and methods’). The dendrogram of morphological similarity between each individual iPN shows that all, except one iPN, could be clustered according to their target region in either the LH-AM or LH-PM area (Figure 3D) which confirms the classification into two major categories. Additionally, we performed a principal component analysis based on the distances of the similarity scores showing that both neuronal classes possess significantly different target areas in the LH (Figure 3—figure supplement 1A; p < 0.001, one-way ANOSIM).10.7554/eLife.04147.010Figure 3.iPNs can be classified according to their projection pattern in three distinct LH zones.


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)

iPNs can be morphologically segregated according to their target and input region.(A) Principal component analysis based on the distances of the similarity scores of all terminal points of each individual iPN in the LH (for details see ‘Materials and methods’). LH-AM iPNs (blue) and LH-PM iPNs (green) form significantly distinct clusters (***p < 0.001, One-Way ANOSIM, Bray–Curtis). (B) Principal component analysis based on the glomerular innervations of each individual iPN in the AL. Again, LH-AM iPNs (blue) and LH-PM iPNs (green) form significantly distinct clusters (***p < 0.001, One-Way ANOSIM, Bray–Curtis).DOI:http://dx.doi.org/10.7554/eLife.04147.011
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Related In: Results  -  Collection

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fig3s1: iPNs can be morphologically segregated according to their target and input region.(A) Principal component analysis based on the distances of the similarity scores of all terminal points of each individual iPN in the LH (for details see ‘Materials and methods’). LH-AM iPNs (blue) and LH-PM iPNs (green) form significantly distinct clusters (***p < 0.001, One-Way ANOSIM, Bray–Curtis). (B) Principal component analysis based on the glomerular innervations of each individual iPN in the AL. Again, LH-AM iPNs (blue) and LH-PM iPNs (green) form significantly distinct clusters (***p < 0.001, One-Way ANOSIM, Bray–Curtis).DOI:http://dx.doi.org/10.7554/eLife.04147.011
Mentions: We next investigated if the spatially regionalized odor-evoked response patterns are reflected in the axonal terminal fields of MZ699+ iPNs in the LH. To analyze these neurons at the single neuron level, we performed neural tracing by employing a genetically encoded photoactivatable GFP (PA-GFP) (Patterson and Lippincott-Schwartz, 2002; Datta et al., 2008; Ruta et al., 2010). The photoconversion of all MZ699+ neurons leaving the AL confirmed the homogeneous distribution of iPN neurites in the LH and the sparse innervation of the posterior-lateral region as mentioned above (Figure 3A). Next we illuminated PA-GFP in single somata to selectively label individual MZ699+ iPNs from the soma up to the farthest axonal terminals in the LH. Individual iPNs were reconstructed and transformed into a reference brain using the END1-2 background (Grabe et al., 2014) to align neurons of different individuals. Based on their innervation pattern in the LH, MZ699+ iPNs could be assigned to two major morphological classes (Figure 3B,C). As expected from the extracted ORDs, one iPN group diverged to the LH-PM region (8/25 of iPNs), while a second group extended their axonal terminations within the LH-AM area (10/25 of iPNs). In order to statistically substantiate our observation, we performed a cluster analysis based on a similarity score (Kohl et al., 2013) of the target areas of all terminals of each iPN in the LH (for details see ‘Materials and methods’). The dendrogram of morphological similarity between each individual iPN shows that all, except one iPN, could be clustered according to their target region in either the LH-AM or LH-PM area (Figure 3D) which confirms the classification into two major categories. Additionally, we performed a principal component analysis based on the distances of the similarity scores showing that both neuronal classes possess significantly different target areas in the LH (Figure 3—figure supplement 1A; p < 0.001, one-way ANOSIM).10.7554/eLife.04147.010Figure 3.iPNs can be classified according to their projection pattern in three distinct LH zones.

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
Related in: MedlinePlus