Visual navigation in ants has long been a focus of experimental study [1][2][3], but only recently have explicit hypotheses about the underlying neural circuitry been proposed [4]. Indirect evidence suggests the mushroom bodies (MB) may be the substrate for visual memory in navigation tasks [5-8],
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.
Insects' aptitude to perform hovering, automatic landing and tracking tasks involves accurately controlling their head and body roll and pitch movements, but how this attitude control depends on an internal estimation of gravity orientation is still an open question. Gravity perception in flying insects has mainly been studied in terms of grounded animals' tactile orientation responses, but it has not yet been established whether hoverflies use gravity perception cues to detect a nearly weightless state at an early stage. Ground-based microgravity simulators provide biologists with useful tools for studying the effects of changes in gravity. However, in view of the cost and the complexity of these set-ups, an alternative Earth-based free-fall procedure was developed with which flying insects can be briefly exposed to microgravity under various visual conditions. Hoverflies frequently initiated wingbeats in response to an imposed free fall in all the conditions tested, but managed to avoid crashing only in variably structured visual environments, and only episodically in darkness. Our results reveal that the crash-avoidance performance of these insects in various visual environments suggests the existence of a multisensory control system based mainly on vision rather than gravity perception.
The ability of hoverflies to control their head orientation with respect to their body contributes importantly to their agility and their autonomous navigation abilities. Many tasks performed by this insect during flight, especially while hovering, involve a head stabilization reflex. This reflex, which is mediated by multisensory channels, prevents the visual processing from being disturbed by motion blur and maintains a consistent perception of the visual environment. The so-called dorsal light response (DLR) is another head control reflex, which makes insects sensitive to the brightest part of the visual field. In this study, we experimentally validate and quantify the control loop driving the head roll with respect to the horizon in hoverflies. The new approach developed here consisted of using an upside-down horizon in a body roll paradigm. In this unusual configuration, tethered flying hoverflies surprisingly no longer use purely vision-based control for head stabilization. These results shed new light on the role of neck proprioceptor organs in head and body stabilization with respect to the horizon. Based on the responses obtained with male and female hoverflies, an improved model was then developed in which the output signals delivered by the neck proprioceptor organs are combined with the visual error in the estimated position of the body roll. An internal estimation of the body roll angle with respect to the horizon might explain the extremely accurate flight performances achieved by some hovering insects.
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