Ants, like many other animals, use visual memory to follow extended routes through complex environments, but it is unknown how their small brains implement this capability. The mushroom body neuropils have been identified as a crucial memory circuit in the insect brain, but their function has mostly been explored for simple olfactory association tasks. We show that a spiking neural model of this circuit originally developed to describe fruitfly (Drosophila melanogaster) olfactory association, can also account for the ability of desert ants (Cataglyphis velox) to rapidly learn visual routes through complex natural environments. We further demonstrate that abstracting the key computational principles of this circuit, which include one-shot learning of sparse codes, enables the theoretical storage capacity of the ant mushroom body to be estimated at hundreds of independent images. We propose a model based directly on insect neuroanatomy that is able to account for the route following capabilities of ants. We show this mushroom body circuit has the potential to store a large number of images, generated in a realistic simulation of an ant traversing a route, and to distinguish previously stored images from highly similar images generated when looking in the wrong direction. It can thus control successful recapitulation of routes under ecologically valid test conditions.

Desert ants make use of various navigational techniques, including path integration and visual route following, to forage efficiently in their extremely hostile environment. Species-specific differences in navigation have been demonstrated, although it remains unknown if these divergences are caused by environmental adaptation. In this work, we report on the navigational strategies of the European ant Cataglyphis velox, which inhabits a visually cluttered environment similar to the Australian honey ant Melophorus bagoti, although it is more closely related to other North African Cataglyphis species. We show that C. velox learn visually guided routes, and these are individual to each forager. Routes can be recalled in the absence of global path integration information or when placed in conflict with this information. Individual C. velox foragers are also shown to learn multiple routes through their habitat. These routes are learned rapidly, stored in long-term memory, and recalled for guidance as appropriate. Desert ants have previously been shown to learn multiple routes in an experimental manipulation, but this is the first report of such behavior emerging spontaneously. Learning multiple paths through the habitat over successive journeys provides a mechanism by which ants could memorize a series of interlaced courses, and thus perform complex navigation, without necessarily having a map of the environment.

Animals travelling through the world receive input from multiple sensory modalities that could be important for the guidance of their journeys. Given the availability of a rich array of cues, from idiothetic information to input from sky compasses and visual information through to olfactory and other cues (e.g. gustatory, magnetic, anemotactic or thermal) it is no surprise to see multimodality in most aspects of navigation. In this review, we present the current knowledge of multimodal cue use during orientation and navigation in insects. Multimodal cue use is adapted to a species’ sensory ecology and shapes navigation behaviour both during the learning of environmental cues and when performing complex foraging journeys. The simultaneous use of multiple cues is beneficial because it provides redundant navigational information, and in general, multimodality increases robustness, accuracy and overall foraging success. We use examples from sensorimotor behaviours in mosquitoes and flies as well as from large scale navigation in ants, bees and insects that migrate seasonally over large distances, asking at each stage how multiple cues are combined behaviourally and what insects gain from using different modalities.

In situations with redundant or competing sensory information, humans have been shown to perform cue integration, weighting different cues according to their certainty in a quantifiably optimal manner. Ants have been shown to merge the directional information available from their path integration (PI) and visual memory, but as yet it is not clear that they do so in a way that reflects the relative certainty of the cues. In this study, we manipulate the variance of the PI home vector by allowing ants ( Cataglyphis velox ) to run different distances and testing their directional choice when the PI vector direction is put in competition with visual memory. Ants show progressively stronger weighting of their PI direction as PI length increases. The weighting is quantitatively predicted by modelling the expected directional variance of home vectors of different lengths and assuming optimal cue integration. However, a subsequent experiment suggests ants may not actually compute an internal estimate of the PI certainty, but are using the PI home vector length as a proxy.

Insect navigation arises from the coordinated action of concurrent guidance systems but the neural mechanisms through which each functions, and are then coordinated, remains unknown. We propose that insects require distinct strategies to retrace familiar routes (route-following) and directly return from novel to familiar terrain (homing) using different aspects of frequency encoded views that are processed in different neural pathways. We also demonstrate how the Central Complex and Mushroom Bodies regions of the insect brain may work in tandem to coordinate the directional output of different guidance cues through a contextually switched ring-attractor inspired by neural recordings. The resultant unified model of insect navigation reproduces behavioural data from a series of cue conflict experiments in realistic animal environments and offers testable hypotheses of where and how insects process visual cues, utilise the different information that they provide and coordinate their outputs to achieve the adaptive behaviours observed in the wild.