Structure and development of the subesophageal zone of the Drosophila brain. II. Sensory compartments

J Comp Neurol. 2018 Jan 1;526(1):33-58. doi: 10.1002/cne.24316. Epub 2017 Sep 28.

Abstract

The subesophageal zone (SEZ) of the Drosophila brain processes mechanosensory and gustatory sensory input from sensilla located on the head, mouth cavity and trunk. Motor output from the SEZ directly controls the movements involved in feeding behavior. In an accompanying paper (Hartenstein et al., ), we analyzed the systems of fiber tracts and secondary lineages to establish reliable criteria for defining boundaries between the four neuromeres of the SEZ, as well as discrete longitudinal neuropil domains within each SEZ neuromere. Here we use this anatomical framework to systematically map the sensory projections entering the SEZ throughout development. Our findings show continuity between larval and adult sensory neuropils. Gustatory axons from internal and external taste sensilla of the larva and adult form two closely related sensory projections, (a) the anterior central sensory center located deep in the ventromedial neuropil of the tritocerebrum and mandibular neuromere, and (b) the anterior ventral sensory center (AVSC), occupying a superficial layer within the ventromedial tritocerebrum. Additional, presumed mechanosensory terminal axons entering via the labial nerve define the ventromedial sensory center (VMSC) in the maxilla and labium. Mechanosensory afferents of the massive array of chordotonal organs (Johnston's organ) of the adult antenna project into the centrolateral neuropil column of the anterior SEZ, creating the antenno-mechanosensory and motor center (AMMC). Dendritic projections of dye back-filled motor neurons extend throughout a ventral layer of the SEZ, overlapping widely with the AVSC and VMSC. Our findings elucidate fundamental structural aspects of the developing sensory systems in Drosophila.

Keywords: Drosophila; RRID:AB_2314331; RRID:AB_528402; RRID:AB_528404; RRID:BDSC_32185; RRID:BDSC_57591; RRID:BDSC_57597; RRID:BDSC_57636; RRID:BDSC_57654; RRID:BDSC_57659; RRID:BDSC_57670; RRID:BDSC_57686; RRID:BDSC_57687; brain; development; gustatory center; mechanosensory center; sensory afferent; subesophageal zone.

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Brain* / cytology
  • Brain* / embryology
  • Brain* / growth & development
  • Cadherins / genetics
  • Cadherins / metabolism
  • Cell Adhesion Molecules, Neuronal / genetics
  • Cell Adhesion Molecules, Neuronal / metabolism
  • Drosophila
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Imaging, Three-Dimensional
  • Larva
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism
  • Microscopy, Confocal
  • Neuropil / cytology*
  • Olfactory Pathways* / cytology
  • Olfactory Pathways* / embryology
  • Olfactory Pathways* / growth & development
  • Pupa
  • Visceral Afferents* / cytology
  • Visceral Afferents* / embryology
  • Visceral Afferents* / growth & development

Substances

  • BRP protein, Drosophila
  • Cadherins
  • Cell Adhesion Molecules, Neuronal
  • Drosophila Proteins
  • Membrane Glycoproteins
  • Nrt protein, Drosophila
  • Nrg protein, Drosophila
  • Green Fluorescent Proteins