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. Recently, Drosophila has been added to the list of insects thought capable of this navigational memory. Existing experimental evidence, however, has a potential confound. Here we show that pheromones deposited at the site of reward might enable flies to find previously rewarding locations even without memory. Thus, 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.

Emergent spatial goals in an integrative model of the insect central complex

“…Here we suggest that PI and vector memory are not just specialised functions for central place foraging, but rather play a more general role, intrinsic to how the CX supports all spatial behaviour. The high degree of conservation in CX structure across insect species and the existence of PI in species such as Drosophila [ 22 , 23 ] support this extension. For example, a simple modification of the circuit—abolition of the return inhibitory pathway—sustains navigation and exploitation of several food sources in a ‘nomadic’ fashion ( Fig 12 ), reminiscent of Drosophila exploratory behaviour [ 81 ].…”

“…At the same time, the conserved nature of the CX circuit suggests it plays a role in the spatial behaviour of all insects, not just central place foragers, species like wasps, bees or ants inhabiting a nest, for which efficient relocation of the nest and food sources by individuals is crucial to survival [ 21 ]. Indeed, path integration has also been observed, over smaller spatial scales, in Drosophila which do not possess a fixed nest or home [ 22 , 23 ]. The existence of homing in “nomadic” insects allows them to revisit a rewarded location, i.e.…”

Neural Networks for Navigation: From Connections to Computations

“…If the fly walks around without finding more food, it will often return to the former feeding site, and if it does not find the food there, it will execute a local search. Optogenetic virtual food can be substituted for real food in this paradigm, giving the experimenter tight control over the location and timing of food encounters (Behbahani et al 2021, Corfas et al 2019, Titova et al 2022). Importantly, these experiments are performed in darkness; thus, the only available inputs to the path integrator are probably proprioceptive cues and/or motor efference copy.…”