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(searched for: doi:10.1146/annurev-ento-042020-102149)
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Ethology Ecology & Evolution, Volume 33, pp 338-358; https://doi.org/10.1080/03949370.2021.1905075

Abstract:
Spatial orientation is essential for all animals that have to successfully change locations during e.g. foraging, homing or migration. Arthropods occupy many different ecological niches and, thus, have evolved a vast number of orientation strategies while moving by air, land, and water. Some of these strategies seem to be rather simple but are perfectly adapted to the behavioural need of an animal. Other strategies are rather complex and require multiple sensory inputs. But what exactly are the fundamental differences between the various strategies and can we define a common terminology that facilitates debates on the underlying orientation strategies exhibited by arthropods? Here, we review examples of spatial orientation behaviours employed by arthropods and provide a unified terminology about their orientation strategies. In addition to behavioural findings, we also consider the current knowledge of the underlying neuronal network to provide a broad and common terminology of orientation strategies. According to our terminology, “spatial orientation” is any kind of directed behaviour. These directed behaviours can be divided into four types of spatial orientation. Non-compass orientation is based on local directional information, e.g. taxis. Compass orientation is based on global compass information, such as the use of a magnetic compass, or a time-compensated sky compass. Egocentric navigation is based on positional information collected en route, e.g. path integration. Geocentric navigation is based on positional information collected on site, e.g. map-based navigation. We highlight examples of diverse arthropod species and discuss controversial explanations of arthropod behaviour in space.
, , , Paul Graham, Barbara Webb
Published: 28 January 2021
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 ellicit 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 optimized cue integration. 1 Author summary In this paper, we modeled the neural pathway allowing insects to perform landmark guided behaviours using their internal compass. First, we observed the intrinsic property of the connectome, extracted from drosophila online database, between the internal compass neurons and the steering neurons to support an oriented behaviour towards a single landmark. Then, we proposed and evaluated an adaptation of the bees path integration neural circuit, to sustain flexible landmark guidance behaviours such as attraction or menotaxis. We showed the model ability to form a memory during the exploration of the local environment to support both innate or learned navigation behaviour using a single landmark in the environment. In addtion, we demonstrated the transformation of a simple goodness/badness signal, from innate or long-term memory pathways, into an oriented steering signal that could be applied to other sensory pathways. Furthermore, by reproducing lesion experiments in the mushroom bodies of wood ants we highlight the consistency of the model with biological observation. We then discuss the different emergent properties and the potential outcome that this local, and operant, memory supports.
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