Displacement experiments provide evidence for path integration in Drosophila

Abstract

Like many other animals, insects are capable of returning to previously visited locations using path integration, a memory of travelled direction and distance. Recent studies suggest that also Drosophila can use path integration to return to a food reward. However, the existing experimental evidence for path integration in Drosophila has a potential confound: pheromones deposited at the site of reward might enable flies to find previously rewarding locations even without memory. Here we show that pheromones indeed can cause naïve flies to accumulate where previous flies had been rewarded in a navigation task. Therefore, we designed an experiment to determine if flies can use path integration memory despite potential pheromonal cues by displacing the flies shortly after an optogenetic reward. We found that rewarded flies returned to the location predicted by a memory-based model. Several analyses are consistent with path integration as the mechanism by which flies returned to the reward. We conclude that while pheromones may often be important in fly navigation and must be carefully controlled in future experiments, Drosophila may indeed be capable of performing path integration.

Exploration and exploitation are flexibly balanced during local search in flies

“…We took advantage of a published dataset (Corfas et al, 2019), where starved flies were stimulated for 1 s by optogenetically activating neurons expressing sweet gustatory receptors (Miyamoto and Amrein, 2014; Miyamoto et al, 2012) whenever they reached a restricted area in the center of a walking arena. In this assay, flies responded with a search around the site of stimulation, which we will term “optogenetic search” (Kim and Dickinson, 2017; Titova et al, 2023). To evaluate which features were shared between real food-induced local search and optogenetic search, we segmented and analyzed trajectories from flies that were stimulated by activating neurons targeted by a Gr43a- and Gr5a-Gal4 line (Corfas et al, 2019).…”

“…Because locomotor adjustments alone cannot explain the larger scale search pattern with persistent returns, we concluded that flies searching for food in the dark used additional strategies to return to the food. It has been suggested that flies use path integration to keep track of the food spot location (Behbahani et al, 2021; Corfas et al, 2019; Kim and Dickinson, 2017; Titova et al, 2023). A common assumption is that the insect head direction (HD) system (Seelig and Jayaraman, 2015) is required for path integration (Heinze et al, 2018; Stone et al, 2017).…”

“…7). Previous studies suggested that flies rely on path integration (Kim and Dickinson, 2017), but can also follow sensory cues emitted by the food spot or deposited by themselves (Baker et al, 2018; Root et al, 2011; Titova et al, 2023; Tsao et al, 2018; van Breugel, 2021). Our findings suggest that flies can still perform local search in darkness without relying on their head direction system or Orco -mediated olfaction.…”

“…Recent technological advances have enabled quantification of increasingly naturalistic behaviors at high spatial and temporal resolution (Alisch et al, 2018; Barlow et al, 2022; Bath et al, 2014; Branson et al, 2009; Mathis et al, 2018). Studies in flies and bees have used these advances to gain insights into navigational aspects of local search in insects, exploring primarily how animals return to a known food source (Brockmann et al, 2018; Corrales-Carvajal et al, 2016; Kim and Dickinson, 2017; Murata et al, 2017; Shakeel and Brockmann, 2023; Titova et al, 2023). Later studies have substituted the real food with optogenetic activation of various sensory and brain neurons, to simplify the assay and identify potential neuronal elements involved in eliciting search (Corfas et al, 2019; Haberkern et al, 2019).…”