CLEMENT, L. | bioRxiv Science

bioRxiv2023

Compensation to visual impairments and behavioral plasticity in navigating ants

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. Significance StatementIf humans look at the world with both eyes, they have no problem to then recognize it with one eye only, and vice-versa. Thus, our way of encoding the world is robust to changes of the visual field. Yet ants do so very differently. Views learnt with two eyes can only be recognized with two eyes, and views learnt with one eye can only be recognized with one eyes (the same eye). However, this rigidity is compensated by a remarkable behavioral flexibility. Upon covering one eye, ants - which can no longer recognize their familiar surroundings - will restart a learning process to store these novel visual inputs in a parallel memory and resume their normal foraging activity.

animal behavior and cognition↗

bioRxiv2022

An intrinsic oscillator underlies visual navigation in ants.

Controlling behavior implies a constant balance between exploration - to gather information - and exploitation - to use this information to reach ones 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 oscillations amplitudes to fit the task at hand in a continuous manner: an unfamiliar panorama enhances the amplitude of oscillations in both naive 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 insects 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.

animal behavior and cognition↗