The navigational skills of ants, bees and wasps represent one of the most baffling examples of the powers of minuscule brains. Insects store long-term memories of the visual scenes they experience, and they use compass cues to build a robust representation of directions. We know reasonably well how long-term memories are formed, in a brain area called the Mushroom Bodies (MB), as well as how heading representations are formed in another brain area called the Central Complex (CX). However, how such memories and heading representations interact to produce powerful navigational behaviours remains unclear. Here we combine behavioural experiments with computational modelling that is strictly based on connectomic data to provide a new perspective on how navigation might be orchestrated in these insects. Our results reveal a lateralised design, where signals about whether to turn left or right are segregated in the left and right hemispheres, respectively. Furthermore, we show that guidance is a two-stage process: the recognition of visual memories, presumably in the MBs, does not directly drive the motor command, but instead updates a desired heading, presumably in the CX, which in turn is used to control guidance using celestial compass information. Overall, this circuit enables ants to recognise views independently of their body orientation, and combines terrestrial and celestial cues in a way that produces exceptionally robust navigation.

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Current opinion in insect navigation assumes that animals need to align with the goal direction to recognise familiar views and approach it. Yet, ants sometimes drag heavy food items backward to the nest and it is still unclear to what extent they rely on visual memories while doing so. In this study displacement experiments and alterations of the visual scenery reveal that ants do indeed recognise and use the learnt visual scenery to guide their path towards the nest while walking backward. In addition, the results show that backward ants estimate their directional uncertainty by integrating multiple cues such as visual familiarity, the state of their path integrator and the time spent backward. A simple mechanical model based on repulsive and attractive visual memories captures the results and explains how visual navigation can be performed backwards.

24Current opinion in insect navigation assumes that animals need to align with the goal 25 direction to recognise familiar views and approach it. Yet, ants sometimes drag 26 heavy food items backward to the nest and it is still unclear to what extent they rely 27 on visual memories while doing so. In this study displacement experiments and 28 alterations of the visual scenery reveal that ants do indeed recognise and use the 29 learnt visual scenery to guide their path while walking backward. In addition, the 30 results show that backward homing ants estimate their directional certainty by 31 combining visual familiarity with other cues such as their path integrator and the time 32 spent backward. A simple model that combines path integration with repulsive and 33 attractive visual memories captures the results. 34 35

Quantifying the behavior of small animals traversing long distances in complex environments is one of the most difficult tracking scenarios for computer vision. Tiny and low-contrast foreground objects have to be localized in cluttered and dynamic scenes as well as trajectories compensated for camera motion and drift in multiple lengthy recordings. We introduce CATER, a novel methodology combining an unsupervised probabilistic detection mechanism with a globally optimized environment reconstruction pipeline enabling precision behavioral quantification in natural environments. Implemented as an easy to use and highly parallelized tool, we show its application to recover fine-scale motion trajectories, registered to a high-resolution image mosaic reconstruction, of naturally foraging desert ants from unconstrained field recordings. By bridging the gap between laboratory and field experiments, we gain previously unknown insights into ant navigation with respect to motivational states, previous experience, and current environments and provide an appearance-agnostic method applicable to study the behavior of a wide range of terrestrial species under realistic conditions.

Controlling behavior implies a constant balance between exploration – to gather information – and exploitation – to use this information to reach one’s goal. However, how this tradeoff is achieved in navigating animals is unclear. Here we recorded the paths of two phylogenetically distant visually navigating ant species (Myrmecia croslandi and Iridomyrmex purpureus) using a trackball-treadmill directly in their habitat. We show that both species continuously produce regular lateral oscillations with bursts of forward movement when facing the general direction of travel, providing a remarkable tradeoff between visual exploration across directions and movement areas. This dynamical signature is conserved across navigational contexts but requires certain visual cues to be fully expressed. Rotational feedback regulates the extent of turns, but is not required to produce them, indicating that oscillations are generated intrinsically. Learnt visual information modulates the oscillation’s amplitudes to fit the task at hand in a continuous manner: an unfamiliar panorama enhances the amplitude of oscillations in both naïve and experienced ants, favoring visual exploration; while a learnt familiar panorama reduces them, favoring exploitation through. The observed dynamical signature readily emerges from a simple neural-circuit model of the insect’s conserved pre-motor area known as the lateral accessory lobe, endorsing oscillations as a core, ancestral way of moving in insects. We discuss the importance and evolution of self-generated behaviors and how such an oscillator has been exapted to various modalities, behaviors and way of moving.

Desert ants are known to rely heavily on vision while venturing for food and returning to the nest. During these foraging trips, ants memorize and recognize their visual surroundings, which enables them to recapitulate individually learnt routes in a fast and effective manner. The compound eyes are crucial for such visual navigation; however, it remains unclear how information from both eyes are integrated and how ants cope with visual impairment. Here we manipulated the ants visual system by covering one of the two compound eyes and analyzed their ability to recognize familiar views in various situations. Monocular ants showed an immediate disruption of their ability to recapitulate their familiar route. However, they were able to compensate for the visual impairment in a few hours by restarting a route-learning ontogeny, as naive ants do. This re-learning process with one eye forms novel memories, without erasing the previous memories acquired with two eyes. Additionally, ants having learnt a route with one eye only are unable to recognize it with two eyes, even though more information is available. Together, this shows that visual memories are encoded and recalled in an egocentric and fundamentally binocular way, where the visual input as a whole must be matched to enable recognition. We show how this kind of visual processing fits with their neural circuitry.