A unified mechanism for innate and learned visual landmark guidance in the insect central complex

Abstract

Insects can navigate efficiently in both novel and familiar environments, and this requires flexiblity in how they are guided by sensory cues. A prominent landmark, for example, can elicit strong innate behaviours (attraction or menotaxis) but can also be used, after learning, as a specific directional cue as part of a navigation memory. However, the mechanisms that allow both pathways to co-exist, interact or override each other are largely unknown. Here we propose a model for the behavioural integration of innate and learned guidance based on the neuroanatomy of the central complex (CX), adapted to control landmark guided behaviours. We consider a reward signal provided either by an innate attraction to landmarks or a long-term visual memory in the mushroom bodies (MB) that modulates the formation of a local vector memory in the CX. Using an operant strategy for a simulated agent exploring a simple world containing a single visual cue, we show how the generated short-term memory can support both innate and learned steering behaviour. In addition, we show how this architecture is consistent with the observed effects of unilateral MB lesions in ants that cause a reversion to innate behaviour. We suggest the formation of a directional memory in the CX can be interpreted as transforming rewarding (positive or negative) sensory signals into a mapping of the environment that describes the geometrical attractiveness (or repulsion). We discuss how this scheme might represent an ideal way to combine multisensory information gathered during the exploration of an environment and support optimal cue integration. In this paper, we modeled the neural pathway allowing insects to perform landmark guided behaviours using their internal compass. First, by copying available details of the neural connectivity between internal compass neurons and steering neurons in the fruit-fly brain, we show this circuit can produce directed behaviour towards a visual landmark. We then propose a mechanism by which this connectivity could be adapted through experience to support flexible landmark guidance behaviours such as attraction or menotaxis, that is, movement in arbitrary directions relative to the landmark. This mechanism allows a simple goodness/badness signal, from innate or long-term memory pathways, to be converted into an oriented steering signal relative to the visual surroundings. Furthermore, by simulating lesion experiments in the mushroom bodies of wood ants we highlight the consistency of the model with biological observations.