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

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., 2017) 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 a 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, (1) the anterior central sensory center (ACSC) located deep in the ventromedial neuropil of the tritocerebrum and mandibular neuromere, and (2) 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.

MDN brain descending neurons coordinately activate backward and inhibit forward locomotion

“…MDNs can induce backward crawling in the limbless Drosophila larva, and persist into adulthood where they can induce backward walking in the six-legged adult fly. This is remarkable because most mechanosensory neurons are completely different ( Kendroud et al, 2018 ; Kernan, 2007 ), although there are some gustatory and stomatogastric sensory neurons that survive from larva to adult ( Kendroud et al, 2018 ). Similarly, most or all the downstream motor neurons controlling crawling (larva) and walking (adult) are different: abdominal motor neurons in the larva and thoracic motor neurons in the adult.…”

Extended Flight Bouts Require Disinhibition from GABAergic Mushroom Body Neurons

“…In honeybees, electrical stimulation of deep SEZ with high current intensity initiated flight [40]. Although the precise sensory inputs to the OA neurons remain unclear, the SEZ receives proprioceptive information regarding feeding from the head, the mouth cavity, and the trunk [41] as well as mechanosensory inputs from thoracic bristles, eye bristles, wings, and halteres [42]. Moreover, in the SEZ, the adult gnathal ganglion receives inputs from descending neurons that connect to the wing and leg neuropil regions in the ventral nerve cord [43].…”

Progressive derivation of serially homologous neuroblast lineages in the gnathal CNS of Drosophila

“…Since ELs are present in MX and LB and show a quite similar projection pattern ( Fig 11A´ ), it will be interesting to a) test the share of both cohorts and b) identify the circuits they are part of. Detailed descriptions of the gnathal neuropil organisation [ 27 , 63 ] lay a good basis to search for potential input and output partners.…”