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

Abstract

The subesophageal zone (SEZ) of the Drosophila brain houses the circuitry underlying feeding behavior and is involved in many other aspects of sensory processing and locomotor control. Formed by the merging of four neuromeres, the internal architecture of the SEZ can be best understood by identifying segmentally reiterated landmarks emerging in the embryo and larva, and following the gradual changes by which these landmarks become integrated into the mature SEZ during metamorphosis. In previous works, the system of longitudinal fibers (connectives) and transverse axons (commissures) has been utilized as a scaffold that provides internal landmarks for the neuromeres of the larval ventral nerve cord. We have extended the analysis of this scaffold to the SEZ and, in addition, reconstructed the tracts formed by lineages and nerves in relationship to the connectives and commissures. As a result we establish reliable criteria that define boundaries between the four neuromeres (tritocerebrum; mandibular neuromere, maxillary neuromere, labial neuromere) of the SEZ at all stages of development. Fascicles and lineage tracts also demarcate seven columnar neuropil domains (ventromedial, ventro-lateral; centromedial; central; centrolateral; dorsomedial; dorsolateral) identifiable throughout development. These anatomical subdivisions, presented in the form of an atlas including confocal sections and 3D digital models for the larval, pupal and adult stage, allowed us to describe the morphogenetic changes shaping the adult SEZ. Finally, we mapped MARCM-labeled clones of all secondary lineages of the SEZ to the newly established neuropil subdivisions. Our work will facilitate future studies of function and comparative anatomy of the SEZ.

Complete connectomic reconstruction of olfactory projection neurons in the fly brain

“…These PNs originate in the subesophageal zone (SEZ) where they form several distinct clusters. A recent survey of secondary lineages in this region did not identify any that give rise to olfactory PNs [86]. Only a minority of subesophageal lineages divide in the larva to form new adult neurons (28/180), and half have stopped dividing by the late embryonic stage [87].…”

Anatomical characterization of PDF‐tri neurons and peptidergic neurons associated with eclosion behavior in Drosophila

“…The single PDF‐Tri neuron arborizes in the prow (PRW = part of the tritocerebrum, Figure e and Supporting Information; Hartenstein et al, ) and flange (FLA = part of the tritocerebrum, Figure f; Hartenstein et al, ) of the SEZ along the midline, with more extensive branches at the ipsilateral sides (Figure e,f). Ramifications are visible in the aMBDL (arrowhead in Figure f) and along the midline in the most dorsal and ventral parts of the SEZ running posterior to close the loop in the most posterior part of the SEZ (GNG in Figure i).…”

The Feeding Connectome: Convergence of Monosynaptic and Polysynaptic Sensory Paths onto Common Motor Outputs

“…The mapping was aided by the fact that the pharyngeal projections enter the SEZ in distinct bundles that can be observed in both light and EM microscopic sections (Figure 5A,B). The AN and the MN each have three bundles (these nerves are formed by fusion of several axon bundles during development (Hartenstein et al 2017), whereas the PaN has just one. The well characterized projections from the external olfactory organ (DOG) to the antennal lobe (AL), for example, use one of the bundles in the AN (Bundle 3 of the AN).…”

“…We then asked how the hugin neuropeptide (Drosophila neuromedin U homolog) circuit, which relays gustatory information to the protocerebrum (Schlegel et al 2016;Hückesfeld et al 2016), would be positioned with respect to the monosynaptic reflex and multisynaptic MB memory circuits. Based on our earlier studies on mapping sensory inputs onto hugin protocerebrum neurons (huginPC) (Schlegel et al 2016;Hückesfeld et al 2016), we were expecting most inputs from the ACp, which is the primary gustatory sensory compartment (Colomb et al 2007;Hartenstein et al 2017). However, most of the huginPC neurons receive inputs from the sensory compartments ACa and AVa, which are the two major monosynaptic compartments that originate from enteric organs.…”

“…The sensory projections were those that ended blindly, whereas the motor neurons were those with somata in the CNS. For sensory inputs, a regionalization of the target areas can already be seen, reflecting the fact that the nerves are fusions of different axon bundles that arise during embryonic development (Hartenstein et al 2017;Kendroud et al 2017). For example, only the AN has sensory projections that extend into the protocerebrum, whereas a major part of the MN sensory projections extend into the ventral nerve cord.…”