Compensation to visual impairments and behavioral plasticity in navigating ants

AbstractDesert 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 naïve 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.