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.
Highlights
To navigate the environment in a way that optimizes their survival and reproduction, animals have evolved sensory systems
Cell bodies of inhibitory projection neurons (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 lateral horn (LH), thereby bypassing the mushroom body calyx (MBc) (Ito et al, 1997) (Figure 1A,B)
Whereas GH146+ excitatory projection neurons (ePNs) are uniglomerular and retain the topographic code in their axonal arrangement (Marin et al, 2002; Wong et al, 2002; Jefferis et al, 2007), most MZ699+ iPNs possess oligoglomerular innervations suggesting that these neurons might not convey precise odoridentity information
Summary
To navigate the environment in a way that optimizes their survival and reproduction, animals have evolved sensory systems. These have three essential tasks: First, the external world has to be translated into an internal representation in the form of an accurate neural map. The neural map has to be readable and interpretable, that is, the generated neural code must allow common attributes to be extracted across stimuli to enable the animal to make the best decisions. The ability to extract features and integrate stimulus modalities have so far mainly been studied in the visual system (Livingstone and Hubel, 1988; Bausenwein et al, 1992; Nassi and Callaway, 2009). We addressed the question of how stimulus features such as odor valence and intensity are coded and integrated within the olfactory system using the model organism Drosophila melanogaster
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