Structure and development of the subesophageal zone of the Drosophila brain. I. Segmental architecture, compartmentalization, and lineage anatomy

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Processing of gustatory information and the control of feeding behavior in insects is executed by neural circuits located in the subesophageal ganglion (SEG) of the brain (Bullock & Horridge, 1965; Cobb, Scott, & Pankratz, 2009; Dethier, 1976; Freeman & Dahanukar, 2015; Schwarz et al., 2017; Scott, 2005; Wang, Singhvi, Kong, & Scott, 2004; Wright, 2016). In addition, command centers for a variety of other behaviors are also situated in the SEG (larval wandering and ecdysis behavior: Dominick & Truman, 1986; Zitnan & Adams, 2000; stridulation: Lins & Lakes‐Harlan, 1994; respiration: Ramirez, 1998; locomotor behavioral choice: Matsuura, Kanou, & Yamaguchi, 2002; reproductive behavior: Certel, Savella, Schlegel, & Kravitz, 2007; Sakurai, Koganezawa, Yasunaga, Emoto, & Yamamoto, 2013; aggression: Zhou, Rao, & Rao, 2008; Andrews et al., 2014; courtship behavior: Auer & Benton, 2016). The SEG consists of the three fused segmental ganglia that innervate the structures surrounding the mouth of the animal. In primitive insects, three separate segments (called gnathal segments) with movable appendages (mandible, maxilla, labium) form the mouthparts of the animal. In flies, the gnathal segments are strongly reduced and structurally modified. Mandibles are essentially absent; of the maxillary appendages, only the small maxillary palps remain; the labial appendages form the fused proboscis (Bryant, 1978; Ferris, 1950). A similar reduction has taken place in the internal structure of the suboesophageal ganglion. For example, the number of neural lineages, which for the thorax amounts to 30 pairs per neuromere (i.e., 90 per three hemineuromeres), is reduced to a total of 14 for all three gnathal neuromeres together (Kuert, Hartenstein, Bello, Lovick, & Reichert, 2014). This reduction is mostly brought about by programmed cell death, which sets in shortly after gnathal neuroblasts have delaminated (Kuert et al., 2014; Urbach, Jussen, & Technau, 2016). Furthermore, commissural axon tracts and overall volume of the subesophageal neuropil are decreased. Furthermore, as a result of the pronounced condensation that affects the fly nervous system as a whole, the subesophageal ganglion is fused with the basal part of the supraesophageal ganglion into a composite domain called the subesophageal zone (SEZ; Ito et al., 2014). Anteriorly, the tritocerebrum (the neuromere innervating the mouth cavity and the gut) has become fully incorporated into the subesophageal zone (Figure 1a). The tritocerebrum contains neural circuits that sense food stuffs in the mouth and integrate this information with input from the viscera (parameters like extension of the gut or nutrient levels in the tissues, which reflect the need for food intake), and then generate a motor output controlling feeding behavior (Dethier, 1976; Rajashekhar & Singh, 1994).
Sensory and motor axons connect to the SEZ via two composite peripheral nerves called labial nerve, and pharyngeal nerve (Figure 1a). The labial nerve, formed by axon bundles of both labial and maxillary origin, enters the central part of the SEZ and carries chemosensory and mechanosensory afferents from the maxillary palps, proboscis and head capsule, and motor axons that move the proboscis. The pharyngeal nerve, which conducts sensory afferents from the mouth cavity and the foregut, enters the tritocerebrum, located at the anterior tip of the SEZ (Rajashekhar & Singh, 1994). Motor axons of the pharyngeal nerve control the pharyngeal dilator muscles (effect suction during feeding), movement of the proboscis, as well as motility of the foregut.
Very little is known about the anatomy and function of the large number of interneurons, which constitute the majority of neurons in the SEZ by far, and whose arborizations form the “association neuropil” compartments surrounding the sensory centers. A multitude of Gal4 and LexA markers is now becoming available (e.g., Jenett et al.
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