A map of sensilla and neurons in the taste system of drosophila larvae

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A major challenge in the field of neurobiology is to find out how animals detect, discriminate, and respond to the huge variety of sensory stimuli in the environment. Reception of those stimuli starts in the periphery, where specialized receptor proteins recognize certain stimuli and translate these into neuronal activity patterns that are then reported to the central nervous system (Chapman, Simpson, & Douglas, 2013).
In insects, the first structures that come into contact with external stimuli, like tastants, are the sensilla on the body surface. These small organs are formed by cuticle structures associated with sensory neurons for the reception of chemical or mechanical stimuli. Sensilla might form long or short hairs, small pegs or shallow domes. Despite variations in form and shape, across insect species structural properties of sensilla were identified that are required for a particular sensory modality (Altner & Prillinger, 1980; Slifer, 1970; Steinbrecht, 1984). The reception of chemical molecules requires contact between the molecule and the specific receptors on the dendritic membrane. Therefore, the cuticle wall of olfactory sensilla invariably is perforated by multiple pores that enable olfactory molecules to enter (Shanbhag, Müller, & Steinbrecht, 1999; Steinbrecht, 1997). Inside the sensillum, the dendrites of olfactory receptor neurons most often are highly branched but might also be unbranched (Shanbhag et al., 1999). In contrast, reception of taste molecules seems to require only a single but larger pore opening that is located at the tip of taste sensilla (terminal pore). The taste‐sensitive neurons do not branch and most often are accompanied by one mechanosensitive neuron (Altner & Prillinger, 1980; Falk, Bleiser‐Avivi, & Atidia, 1976; Slifer, 1970).
The major taste sensilla of cyclorrhaphan fly larvae are supposed to cluster in the terminal organ (TO) at the tip of the cephalic lobes (Figure 1a, b) (reviewed in: Cobb, Scott, & Pankratz, 2009; Gerber & Stocker, 2007). A detailed description of TO ultrastructure was provided by Chu‐Wang and Axtell (1972) for Musca domestica larvae. Hence, the TO consists of 14 external sensilla grouped into five types which divide into a dorso‐lateral group and a distal group. Gustatory function was inferred for most of the sensilla due to relevant structural properties (Chu‐Wang & Axtell, 1972). Investigations on the ultrastructure of the TO of Drosophila melanogaster larvae, however, have been rare (Singh & Singh, 1984). This paucity of information might derive from the technical difficulty to examine sensillar ultrastructure in three dimensions using transmission electron microscopy (TEM). Only recently a number of advanced techniques to effectively acquire volume electron microscopy data have been introduced to the field of biology (Briggman & Bock, 2012; Peddie & Collinson, 2014).
Nevertheless, in Drosophila larvae, a function in taste reception of the TO was confirmed by behavioral, physiological and anatomical studies (Apostolopoulou, Mazija, Wust, & Thum, 2014; Apostolopoulou, Rist, & Thum, 2015; Colomb, Grillenzoni, Ramaekers, & Stocker, 2007; Heimbeck, Bugnon, Gendre, Haberlin, & Stocker, 1999; Kim, Choi, Kang, & Kwon, 2016; Kwon, Dahanukar, Weiss, & Carlson, 2007; Oppliger, Guerin, & Vlimant, 2000; Python & Stocker, 2002; van Giesen et al., 2016). Importantly, a receptor‐to‐neuron map of gustatory receptors (Grs) and neurons of the TO was constructed using the GAL4/UAS system. In this map, eight neurons of the TO are defined by their combinatorial expression of 28 Gr‐GAL4 drivers (Kwon et al., 2007). Subsequent studies assigned a role to mapped TO neurons in the reception of bitter compounds (Apostolopoulou et al., 2014; H. Kim et al., 2016; van Giesen et al., 2016) and also of other tastants (van Giesen et al., 2016). In addition to Grs, neurons of the TO might express Ionotropic receptors (Irs) (Croset et al.
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