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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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Correlation matrices for odor-evoked responses in the AL and LH.Complete correlation matrices for calcium activity patterns of OSNs in the AL (left) and iPNs in the LH (right). The odors are arranged according to single linkage clustering of the AL activity patterns. Heatmap color-code refers to the correlation distance scale bar below each matrix. Odor letters are color-coded according to hedonic valence; 10−6 RI values are labeled in grey (complete list right hand).DOI:http://dx.doi.org/10.7554/eLife.04147.018
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fig6s3: Correlation matrices for odor-evoked responses in the AL and LH.Complete correlation matrices for calcium activity patterns of OSNs in the AL (left) and iPNs in the LH (right). The odors are arranged according to single linkage clustering of the AL activity patterns. Heatmap color-code refers to the correlation distance scale bar below each matrix. Odor letters are color-coded according to hedonic valence; 10−6 RI values are labeled in grey (complete list right hand).DOI:http://dx.doi.org/10.7554/eLife.04147.018

Mentions: Finally, we wondered if this valence-specific LH representation is already reflected at the primary level of olfactory processing. The odor-evoked responses in iPNs are generally similar to those in OSNs (Wang et al., 2014), indicating a straight forward transduction of cholinergic OSN responses. We therefore performed functional imaging of odor-evoked Ca2+ dynamics at the AL input level by expressing G-CaMP3.0 in OSNs using Orco-GAL4 (Larsson et al., 2004) (Figure 6—figure supplement 2). In order to compare the activity patterns at both processing levels, we calculated correlation distances for all pair-wise combinations of odor-evoked response patterns and plotted these with respect to maximal ORD pattern similarity in the LH (Figure 6E). As expected, odor representations in the LH clearly clustered within three separated parts of the matrix, reflecting our observed ORDs. However, this coding similarity could not predict AL activity patterns, even if the correlation matrix was sorted with respect to pattern similarity in the AL (Figure 6—figure supplement 3).


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)

Correlation matrices for odor-evoked responses in the AL and LH.Complete correlation matrices for calcium activity patterns of OSNs in the AL (left) and iPNs in the LH (right). The odors are arranged according to single linkage clustering of the AL activity patterns. Heatmap color-code refers to the correlation distance scale bar below each matrix. Odor letters are color-coded according to hedonic valence; 10−6 RI values are labeled in grey (complete list right hand).DOI:http://dx.doi.org/10.7554/eLife.04147.018
© Copyright Policy
Related In: Results  -  Collection

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

fig6s3: Correlation matrices for odor-evoked responses in the AL and LH.Complete correlation matrices for calcium activity patterns of OSNs in the AL (left) and iPNs in the LH (right). The odors are arranged according to single linkage clustering of the AL activity patterns. Heatmap color-code refers to the correlation distance scale bar below each matrix. Odor letters are color-coded according to hedonic valence; 10−6 RI values are labeled in grey (complete list right hand).DOI:http://dx.doi.org/10.7554/eLife.04147.018
Mentions: Finally, we wondered if this valence-specific LH representation is already reflected at the primary level of olfactory processing. The odor-evoked responses in iPNs are generally similar to those in OSNs (Wang et al., 2014), indicating a straight forward transduction of cholinergic OSN responses. We therefore performed functional imaging of odor-evoked Ca2+ dynamics at the AL input level by expressing G-CaMP3.0 in OSNs using Orco-GAL4 (Larsson et al., 2004) (Figure 6—figure supplement 2). In order to compare the activity patterns at both processing levels, we calculated correlation distances for all pair-wise combinations of odor-evoked response patterns and plotted these with respect to maximal ORD pattern similarity in the LH (Figure 6E). As expected, odor representations in the LH clearly clustered within three separated parts of the matrix, reflecting our observed ORDs. However, this coding similarity could not predict AL activity patterns, even if the correlation matrix was sorted with respect to pattern similarity in the AL (Figure 6—figure supplement 3).

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