Descending control and regulation of spontaneous flight turns inDrosophila

Abstract

The clumped distribution of resources in the world has influenced the pattern of foraging behavior since the origins of life, selecting for a common locomotor search motif in which straight movements through resource-poor regions alternate with zig-zag exploration in resource-rich domains (Berg, 2000). For example, flies execute rapid changes in flight heading called body saccades during local search (Censi et al., 2013; Collett and Land, 1975; Schilstra and van Hateren, 1999; Wagner and Land, 1986), but suppress these turns during long-distance dispersal (Giraldo et al., 2018; Leitch et al., 2021) or when surging upwind after encountering an attractive odor plume (Budick and Dickinson, 2006; van Breugel and Dickinson, 2014). Here, we describe the key cellular components of a neural network in flies that generates spontaneous turns as well as a specialized neuron that inhibits the network to promote straight flight. Using 2-photon imaging, optogenetic activation, and genetic ablation, we show that only four descending neurons appear sufficient to generate the descending commands to execute flight saccades. The network is organized into two functional couplets—one for right turns and one for left—with each couplet consisting of an excitatory (DNae014) and inhibitory (DNb01) neuron that project to the flight motor neuropil within the ventral nerve cord. Using resources from recently published connectomes of the fly brain (Scheffer et al., 2020; Dorkenwald et al., 2023; Schlegel et al., 2023), we identified a large, unique interneuron (VES041) that forms inhibitory connections to all four saccade command neurons and created specific genetic driver lines for this cell. As predicted by its connectivity, activation of VES041 strongly suppresses saccades, suggesting that it regulates the transition between local search and long-distance dispersal. These results thus identify the critical elements of a network that not only structures the locomotor behavior of flies, but may also play a crucial role in their foraging ecology.

Wind Gates Olfaction Driven Search States in Free Flight

“…In the silk moth Bombyx mori , crosswind counter turning is likely generated by pairs ‘flip flop’ neurons in the lateral accessory lobe [Kanzaki and Mishima, 1996]. Saccade directionality and timing in flying flies may be controlled by analogous pairs of neurons [Ros et al, 2023]. Compared to walking moths however, crosswind casting in flies is not simply an alternation of contralateral turns (Figure 3d).…”

“…In the silk moth Bombyx mori , crosswind counter turning is likely generated by pairs ‘flip flop’ neurons in the lateral accessory lobe 44 . Saccade directionality and timing in flying flies may be controlled by analogous pairs of neurons 45 . Compared to walking moths however, crosswind casting turns in flies are not simply large alternating contralateral saccades, but are composed of a more nuanced structure of smaller saccades that together result in crosswind movement (Figure 3d).…”

A central steering circuit inDrosophila

“…LAL013 is presynaptic to several classes of descending neuron (Figure 1q). These descending outputs include DNae014, which has been shown to control saccades made during flight 7 , and DNa02, which contributes to turns made during walking 5,6 . Three other functionally uncharacterized descending neurons also receive strong direct input from LAL013: DNa11, DNae003, and DNa03 (Figure 1q and Figure 2a).…”

“…The specific neurons and circuits in the insect LAL that drive these exploratory turns have not yet been identified. These turns, like those made for course correction, are probabilistic, hinting at the existence of central steering circuits in the LAL that are utilized in both goal-directed locomotion and exploratory behaviour.The DNa02, DNae014, DNb01 and DNg13 descending neurons have all recently been shown to function in turning [5][6][7] . As turning-related activity is wide-spread among descending axons 2 , these neurons likely represent a small fraction of descending pathways that participate in steering control.…”

“…The DNa02, DNae014, DNb01 and DNg13 descending neurons have all recently been shown to function in turning [5][6][7] . As turning-related activity is wide-spread among descending axons 2 , these neurons likely represent a small fraction of descending pathways that participate in steering control.…”