The functional organization of descending sensory-motor pathways in Drosophila

Abstract

In most animals, the brain controls the body via a set of descending neurons (DNs) that traverse the neck. DN activity activates, maintains or modulates locomotion and other behaviors. Individual DNs have been well-studied in species from insects to primates, but little is known about overall connectivity patterns across the DN population. We systematically investigated DN anatomy in Drosophila melanogaster and created over 100 transgenic lines targeting individual cell types. We identified roughly half of all Drosophila DNs and comprehensively map connectivity between sensory and motor neuropils in the brain and nerve cord, respectively. We find the nerve cord is a layered system of neuropils reflecting the fly’s capability for two largely independent means of locomotion -- walking and flight -- using distinct sets of appendages. Our results reveal the basic functional map of descending pathways in flies and provide tools for systematic interrogation of neural circuits.

Multisensory Control of Orientation in Tethered Flying Drosophila

“…The central complex, a region implicated in navigation and turning control [14,49,50], is known to receive both ipsilaterally-tuned input from visual interneurons [48,51] and directional mechanosensory signals [52]. Alternatively, visual and mechanosensory information could converge directly onto descending neurons that target the ventral nerve cord [53], as occurs in neurons that drive escape behavior [54,55]. Finally, it is also possible that visual and mechanosensory signals converge within the ventral nerve cord itself.…”

Extended Flight Bouts Require Disinhibition from GABAergic Mushroom Body Neurons

“…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]. Based on these data, we speculate that OA-VPM4 neurons in the SEZ receive a range of sensory information that includes availability of food sources and food intake, and together, such inputs to the OA-VPM4 interneurons help maintain the fly's ''flight state'' by stimulation of the PAM-DANs.…”

Olfactory and neuromodulatory signals reverse visual object avoidance to approach in Drosophila

“…In house flies, a class of neurons of the lobula plate are excited by motion within a small receptive field and are inhibited by wide-field displacement of the panorama (Egelhaaf, 1985;Liang et al, 2008) but as yet these cells are unknown in Drosophila . Recent studies of the Drosophila lobula have characterized several classes of columnar projection neurons that encode visual features such as looming (Namiki et al, 2018) , movement of small contrasting targets (Keleş and Frye, 2017) , and optical disparities generated by vertical edges moving against a visual panorama that correlate with behavioral reactions to similar single-edge stimuli . How these or other cell classes outside of the T4/T5 directional motion detection pathway participate in object behavior remains to be fully understood.…”