A population of central complex neurons promoting orientation to airflow in Drosophila

Abstract

How brain circuits convert sensory signals into goal-oriented movement is a central question in neuroscience. In insects, a region known as the Central Complex (CX) is believed to support navigation, but how its compartments process diverse sensory cues to guide navigation is not fully clear. To address this question, we recorded from genetically-identified CX cell types in Drosophila and presented directional visual, olfactory, and airflow cues known to elicit orienting behavior. We found that a group of columnar neurons targeting the ventral fan-shaped body (ventral P-FNs) are robustly tuned for airflow direction. Unlike compass neurons (E-PGs), ventral P-FNs do not generate a "map" of airflow direction; rather they are tuned to two directions - approximately 45{degrees} to the right or left of the midline - depending on the hemisphere of the cell body. Ventral P-FNs with both direction preferences innervate each CX column, potentially forming a basis for constructing representations of airflow in various directions. We explored two possible sources for ventral P-FN airflow tuning, and found that they mostly likely inherit these responses via a pathway from the lateral accessory lobe (LAL) to the noduli (NO). Silencing ventral P-FNs prevented flies from adopting stable orientations relative to airflow in closed-loop flight. Specifically, silenced flies selected improper corrective turns following changes in airflow direction, but not after airflow pauses, suggesting a specific deficit in sensory-motor action selection. Our results identify a group of central complex neurons that robustly encode airflow direction and are required for proper orientation to this stimulus.